Cognition, Motivation, Emotion and Action A Dynamic and Vulnerable Interdependence

Applied Animal Behaviour Science 86 (2004) 173–204
Cognition, motivation, emotion and action: a

dynamic and vulnerable interdependence夽
Frederick Toates∗
Open University, Milton Keynes MK7 6AA, UK
Abstract
A model of the interactive processes of cognition, motivation, emotion and action selection is
proposed. Building on earlier theoretical models, it is argued that behaviour is determined by a
combination of ‘on-line’ direct controls and ‘off-line’ cognitive controls. These result in different
modes of behavioural control exhibiting different behavioural properties. Certain similar changes
over phylogeny and ontogeny can be observed in terms of an altered relative weight between these
controls. Under natural conditions, adaptation can be served by a change of weight between different
levels of control as a function of circumstances. It is suggested that under abnormal conditions, e.g. in
certain domestic environments, the change in weight of control can be such as to lead to behavioural
pathology. Conversely, by a focus on different levels of control, the model can also give indications
of good welfare practice.
© 2004 Elsevier B.V. All rights reserved.
Keywords: Motivation; Cognition; Dopamine; Affect; Stereotypies; Welfare
1. Introduction
The notion that the control of behaviour is organized at different levels of the ner-
vous system has a long and distinguished history within ethology, psychology and neu-
roscience (e.g. Taylor, 1958; MacLean, 1970; Hirsh, 1974; Baerends, 1976; Fentress, 1976;
Gallistel, 1980), and models of behavioural control based on this principle are often termed
‘hierarchical’. At a particular time, according to which levels are most involved in the
production of behaviour, the properties of behaviour can change with circumstances.
As a particular model of such hierarchical control in humans, Norman and Shallice (1986)
suggested that there exist banks of ‘low-level’ links between certain stimuli and responses.
夽 The D.G.M. Wood-Gush Memorial Lecture, 36th International Congress of the ISAE, Egmond aan Zee, The
Netherlands, 2002.
∗ Tel.: +44-1908-653323; fax: +44-1908-654167.
E-mail address: f.toates@open.ac.uk (F. Toates).
0168-1591/$ – see front matter © 2004 Elsevier B.V. All rights reserved.
doi:10.1016/j.applanim.2004.02.010
174 F. Toates / Applied Animal Behaviour Science 86 (2004) 173–204
The capacity of stimuli to trigger corresponding responses is modulated top–down by what

they term a ‘supervisory attentional system’. The relevance of this model has been noted very
widely, for example, in the contexts of autism (Turner, 1997), patients suffering from damage
to the frontal lobe (Shallice and Burgess, 1991) and schizophrenia (Crider, 1997) and to
animal stereotypies (Garner and Mason, 2002). Within this tradition of hierarchical control,
the present contribution will continue one strand of theoretical development by building
upon earlier models involving multiple levels of information processing and behavioural
control (Toates, 1995, 1998, 2000, 2001, 2002).
The model that is presented here has certain additions to those of others proposed earlier:
(a) it suggests a relationship between, on the one hand, hierarchical control of motor action
and, on the other, the notions of physiological (‘motivational’) states and emotion;
(b) it links to recent developments in the area of cognition and the neuroscience of moti-
vation, with a particular emphasis upon the animal literature;
(c) it addresses in more detail issues of the possible link between hierarchical control and
stereotypy;
(d) it looks at similarities in principles of behavioural control when comparing humans and
non-humans;
(e) it considers the developmental factors that underlie the emergence of hierarchical control
and the circumstances under which these can ‘go wrong’; and
(f) it suggests that consideration of (a)–(e) could prove to be of central relevance to dis-
cussions of animal welfare. Insight into the processes of behavioural control can help
to give a theoretical rationale to claims regarding such notions as animal boredom and
curiosity, something very close to the heart of David Wood-Gush.
I shall argue that the basis of some behavioural pathology can be identified in terms
of specific distortions of the normal relations between such processes as cognition and
action selection. Although, of course, in applied ethology the primary concern is non-human
species, I shall draw on both human and non-human evidence. To summarize the theorizing,
I shall develop the earlier model of the multi-layered processes underlying the control of
behaviour. The full details of this model and justification for the assumptions built in will
not be repeated here, though a summary of its essentials will now be given.
2. An explanatory model
2.1. Basics of the model
Behaviour is considered here to be all that an animal does in relation to the external
world and is determined by a whole range of different processes encompassing such things
as motivation, emotion, cognition, reflexes and modal action patterns. It is argued that there
are different modes of behavioural control which reflect different levels of organization
within the nervous system. The different modes of behavioural control are revealed in
different properties of behaviour.
Fig. 1 shows a development of a model of the control of behaviour. Various stimuli
impinge upon the animal’s sense organs, e.g. S1 , S2 , S3 . . . As an aspect of the model,
F. Toates / Applied Animal Behaviour Science 86 (2004) 173–204 175
COGNITION
EXPECTATIONS
GOALS
HIGH-LEVEL
EMOTIONAL PROCESSING
A
MOT2
2 LOW-LEVEL 3
EMOTIONAL PHYSIOLOGICAL
PROCESSING STATE
D B
COG MOT1
PROP
S1-R1
INTERNAL
S1 R1 CONSEQUENCES
OF BEHAVIOUR
PROP
S2 R2
EXTERNAL
CONSEQUENCES
MO OF BEHAVIOUR
S3 R3
C
1
Fig. 1. Suggested model of the control of behaviour. S1 , S2 , . . . : stimuli that impinge upon sense organs; R1 ,
R2 , . . . : responses performed; PROP: proprioceptive feedback; MO: motor output linking one efferent signal to
a subsequent one; COG: descending cognitive control of behaviour; MOT1 : influence of such physiological state
(‘motivational’) variables as nutrient, fluid or hormone level on S-R connection; MOT2 : influence of such variables
on cognition. There are ‘external consequences of behaviour’, which feed back to change the external world, e.g.
via route 1 stimulus S3 is altered. There are ‘internal consequences of behaviour’, e.g. via route 3 physiological
state is altered, as in nutrient ingestion. Stimulus information is used as part of cognitive processing, e.g. via route
2. In box D, there is ‘low-level emotional processing’ based directly on certain stimulus properties. This affects
particular stimulus–response links. There is also higher-level emotional processing represented in Box A, based
upon placing stimulus information in context in terms of such things as expectations.
some elements of this stimulus array have a tendency to trigger behaviour directly (e.g. S1
tends to trigger R1 ), a so-called ‘low-level control’, ‘on-line’ control or ‘performance line
control’ (Hirsh, 1974). These terms should not be taken to imply that behaviour in response
to a given stimulus is absolutely invariant. Rather, there is a range of possible variations of
precise motor pattern subsumed under a generic description of the kind “approach cue” or
“turn left”. In the sense of a command to behaviour of this sort and in distinction to other
controls, the model shows a direct line between stimulus and response.
Fig. 1 also shows the storage of ‘off-line’ (or ‘cognitive’) representations of events (Box
A), which are able to influence behaviour indirectly by means of descending pathways
(COG). The term ‘off-line’ means that the control is not part of a direct link from stimulus
to response. The expression ‘cognition’ is used here in the sense of information about the
world that takes the form of representations. In the terms of the present model, cognitions are,
by definition, ‘off-line’ information that can be utilized flexibly in the control of behaviour.
These cognitions (‘higher-level controls’) modulate the efficacy with which stimuli are
able to trigger behaviour (Norman and Shallice, 1986; McDonald et al., 2001) but in certain
cases they can also trigger behaviour themselves. In terms of the present model, the notion
of ‘executive control’, which is currently popular in both human and non-human primate
literatures (Turner, 1997), captures one feature of such off-line control.
Note that certain physiological variables, such as nutrient and sex hormone levels, exert a
role at both high and low-levels (reviewed by Toates, 2001). They play a role, respectively,
in cognition and modulating the efficacy with which certain stimuli can trigger responses.
In terms of representing emotions, the evidence (see Section 5.3) suggests that these arise at
different levels of nervous system organization and thereby after different degrees of neural
processing (LeDoux, 1989; reviewed by Toates, 2002). Thus, in the model, emotions are
represented as arising as a combination of (a) direct stimulus information (Box D) and (b)
more indirectly, stimulus information placed in the context of expectations, etc. (Box A).
As a broad-brush stroke division, the model is based on the assumption that what an
animal does at any point in time depends upon at least three types of factor:
(1) the external stimuli that impinge upon its sense organs at that time, the bases of action
in response to them being represented by such links as S1 –R1 .
(2) High-level cognitions, the influence of which on behaviour is represented by descending
pathways.
(3) What the animal has just done. Thus, a link such as MO represents the influence of
the motor output to R2 exerting an influence on R3 , termed ‘transition biasing’. For
example, consider the rather fixed sequence of behavioural components that constitute
a modal action pattern. It is suggested that this represents in part the outcome of such
a factor. In other cases, in terms of learning, if response R3 repeatedly follows R2
in a particular context, a link of the kind R2 –R3 tends to be formed between them.
Under some conditions, proprioceptive feedback from R2 might also play a role in the
production of R3 .
Different tasks appear to call upon the processes associated with 1–3 to a different extent,
in the sense that the relative weight attached to each process differs with the task. For
example, consider a well-established habit of turning left in a maze. One can postulate a
direct link between the physically-present stimuli at the choice point and the motor act
of turning left, i.e. the weight is upon process 1. Contrast this task with one that involves
delayed responding. Typically, a monkey might be shown two food cups. As it observes
the experimenter, the lid of one cup is raised and the cup is baited with food. Then, after
an enforced delay, the monkey is given a choice of which lid to raise. Such a task cannot
be solved on the basis simply of the physically-present stimuli in the situation, since at the
time of choice these do not differentiate between the two cups. Rather, evidence suggests
that the task is solved on the basis of an internal representation of the world (e.g. ‘the cup to
the left is baited’). A cognition biases to one response and away from another, i.e. weight
is upon process 2.
At any point in time there will be numerous stimuli impinging upon the animal’s sense
organs. Based upon the integration of this information with that contained within stored
representations, there will typically be more than one potential candidate for behavioural
control at any point in time. Thus, necessarily, inhibition upon the behavioural tendency
associated with all but one candidate is implied in any such model. According to the model of
Norman and Shallice, inhibition occurs both between S-R links (‘horizontally’) and from the
attentional/executive regions to modulate the S-R controls (‘vertically’). This assumption
is used in the present model.
A central argument of this presentation is that:
(i) Certain properties of behaviour depend upon the particular relative weight attached to
the factors (1–3 above) as controls of behaviour;
(ii) The relative weight of these factors that is necessary for optimal performance differs
according to circumstances. Changing performance under changing conditions often
reflects such an adaptive shift; and
(iii) Under sub-optimal conditions, as in certain domestic rearing conditions, the weight
distorts, such as to lead to behavioural pathology.
2.2. Changing weight between levels of control
The model suggests that the weight attached to the factors underlying behavioural control
changes as a function of:
(a) Ontogeny and age. With development, the weight of ‘off-line’ controls increases, i.e.
there is an increase in weight of the cognitive system (Bachevalier, 1991). For example,
the growing human infant develops an increasing ability to move the eyes to a posi-
tion of intrinsically low attraction even against the pull of powerful stimuli (Johnson,
1997). Thus, it seems that the capacity to utilize working memory increases with age.
However, in some respects the relationship between age and cognition takes the form
of an inverted-U function. Beyond a certain point, there is a decline in some cogni-
tive abilities with older age. Thus, when challenged to perform some off-line cog-
nitive tasks, older animals tend to revert to an on-line mode of control (Chan et al.,
2002).
(b) Phylogeny. The proposed model is in the spirit of such pioneers as Hughlings Jack-
son (see Taylor, 1958) and MacLean (1970), in suggesting that, in some cases, evo-
lutionary change consists of a ‘grafting on’ of layers of control. It is suggested that
exploitation of certain evolutionary niches is associated with the emergence of par-
ticular cognitive controls. In such terms, primates would appear to have the great-
est capacity to utilize off-line control in the form of working memory in the con-
trol of behaviour, e.g. for complex social dynamics (Diamond, 1996; Goldman-Rakic,
1996).
(c) Learning. With repetition of behaviour under given constant conditions, the weight at-
tached to off-line controls decreases relative to that of more direct processes
(Dickinson, 1985). By contrast, behaviour within a novel environment would be as-
sociated with a stronger weight attached to higher-level controls. Attentional processes
that are engaged in the early stages of learning and which facilitate new association
formations tend to be switched out when a task becomes routine (Pearce et al.,
1998).
(d) Brain damage. Damage to the brain can disrupt one process more than another. Off-line
controls often appear to be particularly vulnerable (Hirsh, 1974). For example, damage
to the prefrontal cortex (PFC) has a particularly disruptive effect on the utilization of
high-level cognition (Passingham, 1993; Diamond, 1996; Goldman-Rakic, 1996). In
the terms of the present article, Parkinson’s disease appears to affect disproportionately
off-line controls as opposed to responses triggered by physically-present stimuli (Kori
et al., 1995). Introducing supplementary (‘guide’) phasic stimuli can assist the patient,
whereas self-initiation of the same response might prove impossible (Evarts and Wise,
1984). With maturation during development, certain reflexes are inhibited. Disease
processes that affect the so-called higher centres (in particular, the cerebral cortex) are
sometimes associated with the reappearance of primitive reflexes (Rafal and Henik,
1994).
(e) Chemical factors. Both endogenous and exogenous chemicals can change the weight of
control. Alcohol tends to decrease the weight of off-line controls (reviewed by Toates,
2002). Catecholamine levels in the prefrontal cortex affect the capacity of an animal to
effect off-line control (Arnsten, 1998).
Having summarized the basic assumptions of a multi-level model, its relevance to un-
derstanding the component processes of cognition, stimulus–response control, motivation
and emotion and their interdependence will be more closely explored.
3. Identifying modes of control and associated brain mechanisms
3.1. Introduction
A model that was designed to represent functional relationships between parts of the
system (Toates, 1998, 2000) will be developed here and shown to dovetail with theorizing
based upon brain structures. Of course, the essence of behavioural control is the inter-
dependence between processes and so it is important to emphasize that behaviour is the
product of multiple interacting processes of the kind described here. The author’s origi-
nal model assimilated a basic and established dichotomy between stimulus–response and
cognitive modes of behavioural control, though it acknowledged that behaviour is often
under both sets of control. A dichotomy between, on the one hand, stimulus–response and
response–response and, on the other, cognitive (‘off-line’) modes of control has served well
as a first approximation in describing the nature of the determinants of behaviour. In some
respects such a dichotomy maps onto a dichotomy of brain structures that underlie con-
trol as revealed by double dissociations following brain lesions (Packard and Knowlton,
2002).
However, researchers in the area of motivation have produced some recent findings that
point to three identifiable levels of brain process (Berridge, 2001; de Borchgrave et al.,
2002; Dickinson et al., 2000) (see Fig. 2). Two of these levels (a and c) map onto the
on-line/off-line distinction in modes of control suggested here but the new research also
Goals,
Cognitions
(c)
(b) RESPONSE
STIMULI PRODUCTION
(a)
RESPONSE
Fig. 2. Brain regions mediating control. (a) Low-level or direct (stimulus–response and response–response) con-
trol, (b) intermediate-level control mediated via dopaminergic VTA-N.acc. ‘incentive salience’ pathway and (c)
high-level cognitive control.
identifies other brain regions that have some contribution to these modes of control but are
less easily allocated to one or other part of the dichotomy.
The suggested three levels of control are as follows:
(a) Low-level control. At the lowest level there is a stimulus–response system, the strength of
linkage of which might be modulated by motivational state. There is also a response →
response process, i.e. response R2 biases towards performing R3 .
(b) Intermediate-level control. Above level (a), there is a dopamine (DA)-mediated pathway
from the ventral tegmental area (VTA) to the nucleus accumbens, which represents what
some describe as an ‘incentive salience pathway’ (Berridge, 2001; de Borchgrave et al.,
2002).
(c) High-level control. At the top of the hierarchy, there is a cognitive system (Berridge,
2001; de Borchgrave et al., 2002). There is conflicting data on the extent to which this
system is dopamine-dependent (Baldwin et al., 2002; Berridge, 2001; Dickinson et al.,
2000).
The role of the intermediate-level pathway remains to be fully elucidated and categorized.
We need to consider the possibilities that it can take responsibility for behavioural control
itself and/or that it has a possible role in each mode of control and in transitions between
modes.
3.2. The stimulus–response and response–response modes of control
3.2.1. Introduction
Stimulus–response control (Dickinson, 1985; Hirsh, 1974) is incorporated in the model
(represented by the links S1 –R1 , S2 –R2 , etc.), as a mode of control in which certain stimuli in
the environment have the capacity to trigger behaviour. There is no representation of future
goals involved in this mode of control and it is therefore not said to involve knowledge of
the cognitive kind.
3.2.2. Learning
In a Skinner box, an animal can learn a simple ‘mechanical’ procedure of a stimulus–
response kind, somewhat like modifying a reflex. In the terms adopted here, such strength-
ening of a stimulus–response association is a form of learning that does not involve
cognition. It was suggested (Toates, 1998, 2000) that simply with repetition, links of the
kind S1 –R1 and R2 –R3 can strengthen, one possible meaning of the term ‘reinforcement’.
Strengthening of the R2 –R3 type of link represents a change in strength of ‘transition
biasing’.
3.2.3. Brain mechanisms

Interpreting the analyses of various authors (e.g. Blackburn et al., 1992; de Borchgrave
et al., 2002; Ikemoto and Panksepp, 1999; Robbins and Everitt, 1992; White and McDonald,
2002), we would associate the S–R part of process (a) of Fig. 2 with, amongst other struc-
tures, regions of the dorsal striatum. In other words, this structure is involved in the direct
and relatively stereotyped reaction to physically-present stimuli. It appears to play a role in
the organization of behaviour where strong links exist between stimuli and responses. The
response–response part might also be expressed similarly.
Strong and rather direct S-R links appear to underlie a number of aspects of behaviour,
e.g. (i) the consummatory phase of behaviour, (ii) the escape reaction to aversive stimuli
such as shock and (iii) corresponding to habit formation, i.e. as a task becomes automatized,
so there is a shift of weight to an S–R route.
Disruption of the nigrostriatal pathway is associated with sensory–motor disturbance (see
Wise and Bozarth, 1987). Damage to the nigrostriatal pathway on one side of the brain causes
circling behaviour (Glick et al., 1976; Marshall et al., 1974; Ungerstedt, 1971). This again
points to it being a site at which there is some modulation of the strength with which stimuli
are linked to responses, this link being unbalanced after damage to the pathway on one
side. Artificial dopaminergic stimulation of the caudate nucleus triggers the performance
of motor stereotypies (Cooper and Dourish, 1990).
3.3. The cognitive mode of control
3.3.1. Introduction
As noted earlier, the term ‘cognition’ is used here in the sense of the storage of knowledge
about the world. Such knowledge can be exploited flexibly, under some circumstances even
in the absence of the objects to which the knowledge relates. The notion of ‘expectation’ is
a central concept in cognition. For example, a representation that food of a certain type and
amount is located somewhere between the window and the door is an example of cognition
(in this case, part of a cognitive map) (O’Keefe and Nadel, 1978). Such knowledge can
be shown to influence appetitive behaviour leading to the goal. When an animal directs
behaviour to such a location, it is not attracted by a physical stimulus per se but rather
utilizes a representation of the world to extrapolate a goal. In the terms of Hirsh (1974),
cognitions can be described as ‘off-line’ information that can be exploited flexibly in var-
ious ways according to circumstances. The term ‘off-line’ summarizes the fact that cogni-
tions involve knowledge about the world and do not intrinsically specify what the animal
should do.
As one example that appears to be explicable by the utilization of cognition, consider
the phenomenon of spontaneous alternation shown by rats in T-maze. That is, if either of
two arms leads to the same goal-box the rat tends to alternate its choice of arm. Controlled
experimentation suggests that this behaviour reflects an alternation, not of motor responses
per se, but of choice of sensory features of the arm, a form of exploration of the most novel
arm (Montgomery, 1952).
As briefly noted earlier, the essence of cognitive control can also be exemplified in solving
tasks that involve a brief exposure to a situation (E), followed by a delay and then a choice
based on a combination of current visual stimulation (C) and a memory of earlier stimulation
(E) (Bachevalier, 1990). Such tasks cannot be solved on the basis of sensory stimulation
alone but involve the more abstract quality of novelty. In primates such tasks are disrupted
by damage to the amygdala and hippocampus.
3.3.2. Learning and cognition

There is evidence that learning can occur at multiple levels and correspondingly take
different forms. Early theorists on animal welfare issues attached much importance to
the possession of cognitive capacities in relation to learning (see, e.g. Wiepkema, 1987).
Quite apart from learning simple stimulus–response links (Section 3.2.2), the animal can
also learn at a cognitive level, i.e. a representation of what action leads to what out-
come. Specifically, in the Skinner box, it can learn an expectation of the kind (make
lever-press) → (food pellet appears) (Berridge, 2001; Bolles, 1972; Dickinson, 1985).
(Such a representation is distinct from a habit of the form ‘stimulus–response’ by which
the animal accomplished at the task can also ‘blindly’ generate the same behaviour of
lever-pressing. For subtle tests on how to distinguish these modes of control, see the paper by
Dickinson.)
The term ‘extinction’ refers to the loss of a response when the biological reinforcer
that is sustaining it (e.g. shock or food) is omitted. Evidence suggests that part of a
high-level in the hierarchical architecture is involved in extinction (for logic, see Toates,
2002). Learning of a simple relationship between, say, a tone and a fear shown to shock
that has been paired with the tone, appears to be mediated by a direct process. How-
ever, extinction of this relationship (i.e. the loss of fear when the shock is omitted but
the tone still applied) is associated with off-line controls that modulate the on-line con-
trol in a way that can override its influence. It is suggested that the basis of extinction is
the animal’s utilization of a cognition (e.g. that shock no longer follows the tone or that
the previously rewarded goal-box is no longer associated with reward) in the control of
behaviour.
3.3.3. Brain mechanisms

Such structures as the hippocampus and prefrontal cortex have been implicated in what is
termed here ‘cognitive control’ (Bachevalier, 1990; Balleine and Dickinson, 1998; Berridge,
2001; Hirsh, 1974; Rumbaugh, 1997). The cognitive system develops relatively late and
involves interaction between these two structures (Rose, 1980). By contrast, an early de-
veloping S-R system is largely spared following damage to these regions and is thought to
be mediated by a neural circuit involving more posterior regions of the cortex and a basal
ganglia structure, the striatum (Bachevalier, 1990).
Viewed in phylogenetic terms, advanced cognition is associated with a considerable de-
gree of emancipation from stimulus–response learning and control (Rumbaugh, 1997). The
evidence suggests that, with phylogenetic enlargement of the PFC, an increased weight is
attached to off-line controls in newer parts of the cerebral cortex, relative to both older
parts of the cortex and subcortical structures. Of course, cognition is only of adaptive
value provided that, at some stage, it can influence action (i.e. via the descending links
in Fig. 1). There are links from PFC to the basal ganglia, e.g. striatum, and by its influ-
ence there, the PFC plays a role in the control of behaviour (Iversen, 1977; Passingham,
1993; Rolls, 1999). Lesions to the PFC are followed by increased activity and difficulty
in withholding responding in situations earlier associated with reward. Damage to the
PFC–striatal system also causes hungry rats to show elevated activity (Dunnett and Iversen,
1981). As a means of exerting control, the hippocampus appears to mediate between ex-
ecutive regions and such ‘lower-level’ structures as the nucleus accumbens (Christie et al.,
1987).
Spontaneous alternation depends upon the PFC and regions of the striatum with which
it connects (Dunnett and Iversen, 1981). In keeping with theorizing about the role of these
structures, the PFC appears to play a role in the retention of a memory of the last choice
made, which is then placed ‘on-line’ at the striatum in controlling behaviour. This involves
a representation of the world (‘the last choice’) controlling current behaviour, though alter-
nation cannot always be assumed to reflect high-level control (Bubois et al., 1995).
Again pointing the notion of cognition and its role in off-line control, Passingham (1993,
p. 87) notes that
. . . the medial premotor cortex plays a role in the selection of movements when there is
no external cue to tell the subject when to move and what to do. These situations have
been described in the literature as involving ‘self-initiated’ movements or movements
that are determined by ‘internal’ cues.
The PFC selects goals but not the means used to achieve them. This is done lower in the hi-
erarchy. Damage to area 46 of PFC disrupts goal-seeking when a physical stimulus is absent
(e.g. in delayed responding) but not when it is present (choice made to a physically-present
stimulus).
Both extinction and reversal (changing the conditions so that the rewarded condition is
no longer rewarded and the previously unrewarded condition is now rewarded) take longer
in hippocampally-lesioned rats, again indicative of greater persistence (in these cases in the
face of no reward) (Hirsh, 1974; Tracy et al., 2001). Extinction of a learned behaviour can
also be prolonged by lesions of the PFC–striatal system (Dunnett and Iversen, 1981).
3.4. The ventral tegmental area—nucleus accumbens pathway
3.4.1. Introduction
Concerning process (b), activation of the VTA → N.acc. route appears to accentuate the
tendency of the animal to engage actively in approaching stimuli in its external world. This
is exemplified by such things as (a) physically-present stimuli tending to be pursued where
there is not necessarily an existing strong link between the stimulus and a particular response,
(b) conditional stimuli associated with incentives increasing the strength of an associated
behaviour (Berridge, 2001; Blackburn et al., 1992; Ikemoto and Panksepp, 1999; Robbins
and Everitt, 1992; Van den Bos et al., 1991) and (c) novel objects triggering exploration
(see later).
One situation in which the role of activity in the pathway is particularly evident is in
amplifying the power of secondary incentives (e.g. a lever in a Skinner box) to engage
behaviour when reward is relatively infrequent (Salamone et al., 2001). Activation of
this pathway appears to bias animals towards activity, thereby opposing the possible al-
ternative strategy of passivity (Spruijt et al., 2001; Van den Bos and Cools, 1989). This
pathway plays a role in the organization of flexible approach (‘appetitive phase’) and
avoidance of aversive situations. Rather than fixed motor stereotypy, microinjection of
a DA agonist into the N.acc. causes heightened activity, involving approach-investigation
(Cooper and Dourish, 1990; Ikemoto and Panksepp, 1999; Joyce and Iversen, 1984). Ike-
moto and Panksepp suggest that, with repeated experience in a given situation, control
by the N.acc. system gives way to control by the S.Nig.-caudate nucleus (i.e. process a
above). Well-trained animals can still find their way to incentives even in the absence of
the N.acc. (Ikemoto and Panksepp, 1999), i.e. there is a shift of weight away from route b
above.
Route (b) is open to modulation by such states as energy depletion. Two sources of modu-
lation of this route, acting at pathways running to the nucleus accumbens, are the prefrontal
cortex and the hippocampus (cf. Hirsh, 1974). Evidence suggests that energy states affect
the degree to which the hippocampus exerts modulation over the nucleus accumbens (Tracy
et al., 2001).
The VTA → N.acc. system appears to activate (‘energize’) behaviour directed to at-
taining goals, i.e. reward-related stimuli. The evidence strongly points to this DA-mediated
pathway being involved only in the wanting aspect of goal-directed activity and not the
liking aspect of direct engagement with incentives (described later) (Berridge, 2001). Thus,
blocking of DA reduces the animal’s attempts to gain a reward but does not reduce the
impact of the reward, the so-called ‘hedonic effect’. Attempts to tie welfare to the notion
of affective state and the assumed rationality of choice by animals need to take this into
account (cf. Spruijt et al., 2001).
From studies on rats, the VTA-N.acc. route appears not to be involved directly in the
mode of cognitive control (de Borchgrave et al., 2002), whereas, as noted in Section 3.2.3,
the prefrontal cortex appears to be crucially involved in mediating such expectations that
are exploited in goal-directed activity (Balleine and Dickinson, 1998). A non-DA-mediated
process involved in the Skinner box might explain the observation that DA-antagonists take
a long while to exert any effect on operant behaviour whereas approach to an incentive is
immediately disrupted (see Blackburn et al., 1992).
3.4.2. Aversive situations

The VTA-N.acc. route is involved not only in appetitive behaviour but also aversively-
motivated behaviour. Dopaminergic activity in the VTA-N.acc. pathway biases towards
active avoidance and away from the passive response of freezing. Dopamine blockade
disrupts pre-emptive avoidance reactions but does not prevent escape reactions to aversive
stimuli (Blackburn et al., 1992).
There is an antidepressant action of drugs that boost DA activity in the VTA-N.acc.
pathway in that they are followed by a move away from passivity (Willner, 1997). Ikemoto
and Panksepp predict that in learned helplessness there should be a decline in release of
DA from the N.acc. as the animal acquires the cognition of helplessness. The stress of
social defeat and isolation are associated with a loss of incentive motivation as indexed
by appetitive behaviour triggered by a cue predictive of reward (Von Frijtag et al., 2000).
Changes in VTA-N.acc. dopamine seem a likely candidate as the biological basis. The
probability of freezing is less in a novel situation, which suggests that dopamine activation
triggered by novelty biases towards active responses. The reduction of incentive motivation
as a result of stress is one possible index of negative welfare (Spruijt et al., 2001; Von Frijtag
Drabbe Künzel, 2001).
4. Competition between levels of control
4.1. Introduction
At any point in time there will often be more than one candidate for behavioural control
simultaneously present, i.e. there is competition for control. Clearly, the performance of a
single coherent unambiguous sequence of behaviour implies action selection and inhibition
on all but the winning candidate.
According to the analysis presented so far, there are various types of candidate for the
control of behaviour. Thus, the strength of these candidates arises from such things as (1)
physically-present external stimuli, (2) ‘intrinsic’ off-line cognitions (Van den Berken and
Cools, 1982) and (3) links between a response just performed and the trigger to action
(summarized as MO or R2 –R3 in Fig. 1) (Graybiel, 1998). In addition to 1–3, it appears
that intrinsically generated timing signals trigger such activities as dust-bathing in fowl
(Vestergaard, 1980).
An implication of the present analysis is that levels (b) and (c) must be capable of
overriding the more ‘automatic’ response production processes organized at level (a). A
capacity for (action) → (outcome) learning appears to be an evolutionary development that
can override a tendency to, say, superstition (i.e. responding even when it yields little no
reward) that is based on stimulus–response (‘contiguity’) learning (Balleine and Dickinson,
1998).
In the terms of Spruijt et al. (2001), when the animal is in the situation of decision-making,
the system that performs the calculation of cost-benefit has the capacity to compare dif-
ferent expected outcomes. The outcome that appears to offer the highest potential yield
will normally assume control of behaviour. This implies a hierarchical structure with an
inhibition exerted on all but the winning candidate.
4.2. Brain mechanisms
Under some conditions, higher-level controls are capable of overriding lower-level con-
trols. For example, pathway (b), the N.acc. route, can exert inhibition on pathway (a), the
Nig.Striatal pathway (Robbins et al., 1990).
A contemporary understanding of the role of the basal ganglia is in terms of the modulation
of candidates for behavioural control, resolving competing demands for action and providing
an output signal for coherent action (Gonzalez et al., 2000; Greer and Capecchi, 2002; Rolls,
1989; Matthyse, 1974; Van den Berken and Cools, 1982). The basal ganglia exert inhibition
on motor outputs but, when a candidate for action arises, inhibition is lifted from just this
one. All other competitors remain inhibited. The basal ganglia inhibit at both a cortical and
brainstem level (Bradshaw, 2001).
Inputs from the prefrontal cortex appear to bias control at the basal ganglia in favour
of, say, cognitions (e.g. signals of delay, restraint) (Diamond, 1996; Goldman-Rakic, 1996;
Partiot et al., 1996). As an example of a link between cognition and action, the basal ganglia
mediate between a (high-level) command to accelerate running speed and the necessary
(low-level) change in frequency of a central pattern generator. The latter is based in the
brainstem and spinal cord and controls leg movements (Jaspers et al., 1984). Lesions of the
particular regions of the input side of the basal ganglia have a similar effect to lesions of the
regions of prefrontal cortex that project to them. For example, both types of lesion disrupt
a number of what are, in terms of the present analysis, cognitively mediated tasks such
as delayed alternation, withholding responses or performing reversals of choice (Dunnett
et al., 1999; Rolls, 1989). In one mutant mouse model, it appears that the basal ganglia
give an abnormally high weight to the candidacy of grooming signals (Greer and Capecchi,
2002). Mice of this mutant form groom until there is tissue damage.
One role of basal ganglia dopamine appears to be to set the sensitivity of response selec-
tion (Rolls, 1989) or to modulate the signals provided by candidates based on experience. It
appears that incoming signals trigger the nigrostriatal DA system which modulates the effi-
cacy with which candidate signals from the cortex are able to gain expression in behaviour,
a learning function (Doya, 2000).
It is suggested that in the case of modal action patterns, chains of responses can be formed
by means of transition-biasing of components (e.g. R2 –R3 ) at the level of the basal ganglia.
4.3. Some examples of competition for control
4.3.1. Introduction
This section looks at some examples of behaviour for which it is suggested that insight
can be gained by considering multiple levels of control with competition being exerted
between levels.
4.3.2. Activity levels

Hippocampal lesions appear to remove a source of inhibition (control within route c)
and increase locomotion (dependent upon route b) (cf. Hirsh, 1974). Activity in a context
earlier associated with food is increased in rats with hippocampal damage (Tracy et al.,
2001). One role of the hippocampus appears to be that of modulating the efficacy of the
Fig. 3. Experiment that places levels of control in competition. (a) Learning phase. On running from south to
north, the rat is trained to receive food in the goal-box by turning west. On being released from the north end (b),
learning a cognition will take it west (c) whereas a stimulus–response link will take it east (d) (from Toates, 2001).
VTA-N.acc. route (‘incentive motivation pathway’) according to context and particular

current circumstances. For example, by means of this route, some restraint appears to be
exerted on behaviour, based upon off-line processing.
A number of tasks implicate the hippocampus as having a role in exerting inhibition
(Altman et al., 1973; Hirsh, 1974). For example, in a situation of low reward rate (one
in which every lever-press contributes to the gain of reward but where there is a high
effort/reward ratio), hippocampal rats show greater persistence than controls, suggesting a
loss of inhibition (Schmelzeis and Mittleman, 1996).
4.3.3. Mazes
Can one level of control clearly be pitted against another? According to an interpretation
of classical accounts within experimental psychology, level (a) is pitted against higher-levels
(i.e. c) when an animal learns a T-maze task as in Fig. 3a and then is released from the
north end, i.e. Fig. 3b (see Hirsh, 1974; White and McDonald, 2002). The S-R system
will tend to send it East. This behaviour is the result of a stimulus–response link between
the choice point and a motor turn to the left. The cognitive system will tend to take it
West. This involves extrapolation on the location of the goal-box based upon a cognitive
representation of the environment and the tendency to pursue a goal irrespective of the
mechanical response involved. As the length of experience in this apparatus increases, so
there is a shift of weight from cognitive control to stimulus–response control (Packard and
Knowlton, 2002; White and McDonald, 2002). In this experimental design, hippocampal
lesions increase the candidacy of the S-R system whereas lesions of the dorsal striatum tend
to increase the candidacy of the cognitive system.
The radial maze (Olton et al., 1979) can also be used to illustrate a competition be-
tween levels of control. Normally each of eight arms contains a morsel of food at its far
end. In a win-shift task, in order to optimise intake, the animal needs to avoid repeat-
ing a visit to an arm just depleted. By contrast, in a win-stay task, the animal needs
to repeat a visit to an arm just depleted. Hippocampally-lesioned rats are deficient at
win-shift tasks but better than controls at win-stay tasks (see White and McDonald, 2002).
A win-shift task requires the animal to resist the pull of a location just associated with
ingestion and instead to forage elsewhere. In the terms adopted here, a level (b) control
(VTA-N.acc. or ‘incentive approach system’) would tend to pull the animal to repeat its
previous behaviour (‘win-stay’) whereas a cognitive system (c) would motivate it to forage
elsewhere (‘win-shift’).
4.3.4. The ‘misbehaviour’ of organisms

The term ‘misbehaviour’ was famously applied by Breland and Breland (1961) to describe
a series of particular test situations in which tokens were used to obtain food. For example,
a racoon was required to insert a coin in a slot to gain food. At first, things went well and the
animal deposited the coin in the slot and obtained reward, in accordance with behaviourist
principles of reinforcement. However, later behaviour started to ‘degenerate’ in that the
animal found it difficult to let go of the token and deposit it. Thus, the term ‘misbehaviour’
describes the behaviour in which well-learned instrumental behaviour after a while starts to
degenerate. The animal comes to direct its foraging behaviour at the token needed to gain
reward rather than fulfilling the requirement to gain reward, which would consist of letting
the token go by inserting it in the apparatus.
The misbehaviour experiment is widely cited in both pure and applied behavioural science
literatures, as an instance of the ‘constraints on learning’ and the need to take species-typical
behaviour patterns into account (e.g. Mason and Mendl, 1997; Wiepkema, 1987). A sug-
gestion in terms of the present model is that a level (c) action → outcome cognition is
involved in solving the task but that such control by this level is overridden by a level (b)
control as a result of repeated pairing of token and food.
Another instrumental learning situation, studied by Tomie (1996), also appears to pit level
(b) and (c) against each other. A cue light is presented simultaneously with the delivery of
reward but the location of this light is somewhere other than at the manipulandum (e.g. in
the case of a Skinner box, not at the lever). In this condition, a range of different species
finds it difficult to acquire the behaviour of reacting to the manipulandum (relative to when
the cue light is not presented). To do so would involve resisting the lure of directing their
behaviour at the stimulus of the cue light. Following Tomie’s analysis of these phenomena,
we would associate process (b) with such cue-directed behaviour. This presumably means
that such instrumental response directed at the manipulandum as does occur (if any) is
under the control of a type c process. In primates, a developmental effect is seen: increasing
age is associated with increasing ability at this task, i.e. a strengthening of the type (c)
process.
5. Affect and emotion
5.1. Introduction
Closely associated with cognition, are the notions of emotion and affect. Theorists find
it difficult to disentangle exactly what the difference is between these terms, so the use here
can only be provisional. The term ‘affect’ is generally used to refer to a state of the nervous
system that results from current behaviour, e.g. the affect induced by ingesting a palatable
solution.
Spruijt et al. (2001) discuss the capacity of an animal to perform cost-benefit analyses of
the expected outcome of actions prior to their execution. They assume that:
(a) such calculations are given an affective weighting depending upon the utility of the
expected outcome,
(b) (i) expected outcome is compared with (ii) actual outcome, and
(c) disparity between (i) and (ii) is a trigger to emotion/affect.
In terms of the present model, such cost-benefit analysis would engage off-line processing.
5.2. Affect
Opioids doubtless play several roles in the kinds of system under consideration here
(Steiner and Gerfen, 1998) and one such role may be closely involved with the rewarding
effect of consummatory behaviour (‘affect’). This refers to the liking part of the want-
ing/liking dichotomy, the wanting part being discussed in Section 3.3.1. As Spruijt et al.
(2001, p. 153) express it:
Opioid systems seem to act more in ‘the here and now’ when the organism is facing an
environmental challenge to evaluate ongoing behaviour.
In such terms, an opioidergic process would modulate the DA system of wanting so that
it normally reflects liking but there is the possibility of a fracture line between these two
processes.
Pain is an example of affect taking a negative value.
5.3. Emotion
5.3.1. Introduction
As with the other processes already described, evidence points to multiple levels of
process involved in emotion: cortical and subcortical (Lane, 2000; LeDoux, 1989; Toates,
2002).
5.3.2. How emotions arise

Concerning how emotions arise, Fig. 1 shows both low- and high-level computation of
emotion.
Thus, at a low-level, certain stimuli per se (e.g. loud sounds) directly trigger emotions
by a direct route to the amygdala (LeDoux, 1989) (Box D). However, at a higher-level,
stimuli are placed in context in the determination of emotion (Box A). As an example of
such a contextual factor, emotions arise in part from differences between the expected state
of the world and the actual state. As an instance of this, in rodents, the omission of an
expected reward is associated with the emotion of frustration (Gray, 1987) and activation of
the hypothalamic pituitary adrenocortical system (Coover et al., 1971). This illustrates the
generation of emotion following some cognitive computation. The outcome of ‘no food’
is only a trigger to frustration in the context of an expectation of food. This aspect of the
model might prove relevant to attempts to link positive welfare to meeting expectations and
to associate negative welfare with frustration (cf. Spruijt et al., 2001).
For another example of the role of emotion, behavioural control and the implication of a
cognitive factor, consider an experiment in which rats first learn to run for a large reward and
then this is switched to a smaller reward. After the switch, control rats slow their running
speed to a value that is slower than that of rats receiving the smaller reward throughout, a
so-called ‘negative contrast effect’ (Flaherty et al., 1998). This suggests that actual reward
is compared with an expectation based upon experience and this expectation connects
with behavioural control. Placed in this situation, rats with damage to the hippocampus
do not slow up. This suggests that the still-intact incentive motivation based system (level
b) is triggered by physical cues of the maze and the system does not take into account a
revised representation of the goal-object, i.e. a smaller reward. That is to say, a layer of
cognitive control appears to be inoperative as far as the control of behaviour is concerned.
A similar conclusion arises from the observation that, unlike controls, rats with damage
to the hippocampus do not show an elevation in corticosteroid secretion when reward is
omitted in a Skinner box (Coover et al., 1971).
In primates, considerable high-level emotional processing is carried out in the PFC (Rolls,
1999), in the present terms this is off-line (Damasio, 2000). Evidence from non-human
primates shows that the current significance of a conditional cue associated with a primary
reinforcer is computed in the PFC region. Such PFC processing is able to keep pace with
rapid changes in the significance of environmental cues, as when the cue associated with
reward and non-reward are reversed. Subcortical emotional processing is more sluggish
(Rolls, 1999). In the language of hierarchy, the newer (‘hierarchically higher’) structures
exert a modulatory role over the older (‘lower’) structures.
5.3.3. What emotion does

Concerning what an emotion does, the term is used here to describe certain states of the
CNS that play a role in the co-ordination of cognition, internal physiology and external
behaviour. For example, a state of fear simultaneously underlies (a) excitation of escape,
avoidance or freezing and (b) inhibition upon appetitive behaviour. By means of emotion,
behaviour is given a bias towards a limited range of options (e.g. fear biases to fleeing or
freezing).
The model is based on the evidence that emotion serves roles in both high and low-levels
of hierarchical processing. At a high-level, emotion influences decision-making, e.g. fear
biases decision-making towards freezing or avoidance/escape. At a low-level, it modulates
the strength of such reflexes as that of startle (Davis, 1992).
So much for the adult nervous system and behaviour, we now turn to a consideration of
the developmental factors that lead to the adult.
6. Developmental effects
6.1. Introduction
The multi-layer model of behavioural control can yield insights into development, in this
context the central thesis of the present article being as follows:
(1) The development of off-line controls (e.g. in prefrontal cortex) depends upon early
experience. In human infants, the period of about 12–18 months is crucial for neural
differentiation and subsequent emotional regulation (Schore, 1994). Infant rats and
infants of the lagomorph species Octodon degus reared in isolation show abnormal levels
of prefrontal catecholamines (Hall, 1998; Poeggel et al., 2003). In mice, isolation and
food deprivation appear to change the weighting between mesocortical (VTA-PFC) and
mesoaccumbens (VTA-N.acc.) dopamine transmission triggered by stressors (Cabib
et al., 2002);
(2) The relative weight attached to off-line and on-line controls depends upon a develop-
mental history, which for social species involves the dynamics of social contact (e.g.
play) (Schore, 1994). The reaction to novelty is influenced by developmental history.
The ability to assimilate a representation into memory and thereby to show a decrement
in exploration of a given object is a function of early experience (Zimmermann et al.,
2001);
(3) An abnormal relative weight between on-line and off-line controls can arise from ab-
normal long-term environmental factors (e.g. isolation rearing); and
(4) Such an abnormal weight can form one of the bases of behavioural abnormality (e.g.
stereotypies).
A number of different pieces of evidence all points to the same conclusion: early depri-
vation is associated with a decreased capacity to exert off-line control and thereby a bias
towards behaviour being determined by lower-level controls.
6.2. Deprivation effects
In social species, normal development appears to depend upon the facility for exhibiting
flexibility of behaviour in the early social situation. For example, social development and
social play involve the rapid changing of roles and inhibition being exerted on the ‘serious’
completion of certain behaviour sequences (e.g. fighting) (Einon et al., 1977).
A central argument of the present paper is that early social deprivation can lead to a
syndrome of abnormal effects, each of which can be characterized by a lowered sensitivity
of off-line controls and thereby an increased relative sensitivity of on-line controls. That is
to say, the animal’s reaction is to be understood as more strongly dependent upon stimuli
per se, taken out of context. Not all of the effects invariably appear and there exist strain
differences but there is some trend seen (Geyer et al., 1993; Varty et al., 2000). This section
will look at the evidence for this.
Evidence suggests that early deprivation of social play does not disrupt the ability to
express behaviours such as mating and aggression per se. However, it disrupts the ability
of contextual stimuli to modulate the occurrence of behavioural expression (Vanderschuren
et al., 1997). For rats reared in social isolation, there is evidence of a deficiency of inhibitory
control, as revealed by such things as enhanced responding during extinction (Morgan et al.,
1977) and difficulty in withholding responding in order to obtain reward (Morgan and Einon,
1975). Early social isolation is associated with later elevated levels of object investigation
and relatively slow habituation (Einon and Morgan, 1976; Varty et al., 2000). Rearing rats
in social isolation creates indices of stress and the animal develops a deficiency in gating
stimuli. That is to say, it tends to respond in a way determined by the intrinsic properties
of the stimulus taken out of context (Stevens et al., 1997; Varty et al., 2000). Speculatively,
this could be interpreted as a deficiency in the assimilation of features of the world into
an internal representation and/or the use of such representation. There is evidence pointing
to an involvement of dopamine abnormalities, e.g. in the striatum, underlying these effects
(Lewis et al., 1996). Antipsychotic drugs appear to alter the ratio of DA activity between
subcortical and cortical sites (Cohen and Servan-Schreiber, 1992) and partly correct the
influence of early social isolation (Varty et al., 2000).
Social deprivation of primates involves a syndrome, one feature of which is the tendency
to stereotypy (Harlow and Harlow, 1962). Other features are indicative of impaired social
cognition and include a lack of normal social interaction, e.g. sexual invitations are not
reacted to, threat by a dominant would not produce normal withdrawal but in other situa-
tions excessive fearfulness is shown. There is a poor integration of components of motor
performance into a whole pattern, e.g. concerning mating (Mason, 1968). Monkeys raised
in isolation exhibit increased stereotypy, self-mutilation and signs of dopamine hypersen-
sitivity, as indexed by the elevated level of stereotypy following application of a dopamine
agonist (Lewis et al., 1990). Dopaminergic systems within the striatum are compromised
(Martin et al., 1991).
Early socially-deprived rhesus monkeys exhibit a tendency to respond to redundant
stimuli, implying a deficit in the ability to modulate their role as controls of behaviour
(Beauchamp et al., 1991; Lewis et al., 1996). In an instrumental task, chimpanzees with an
experience of social deprivation during early months exhibit perseveration of responding,
i.e. they continue to respond even if the response does not yield reward. That is, relative to
naturally-reared animals they benefit less from the experience of non-reward (Davenport,
1979).
7. Age effects
Siwak et al. (2001) found that the ability of some dogs to perform off-line cognitive
tasks declined with age. Such dogs were also prone to relatively high-levels of activity,
a tendency to stereotyped responding and a low-level of investigative exploration. Siwak
et al. speculated that changes in the prefrontal cortical–striatal–pallidal system formed
the basis of the changes in behaviour. Also, in primates, there is some decline in such
cognitive ability with age, associated with changes in the prefrontal cortex (Tsuchida et al.,
2002).
Having considered the bases of a model of behaviour its relevance to issues of animal
welfare will now be explored in more detail.
8. Exploration and boredom
Exploration was a topic close to the heart of David Wood-Gush (e.g. Wood-Gush et al.,
1983). Of special concern to applied ethologists are observations such as that, placed in a
semi-natural enclosure and given large amounts of food, pigs still spend a high percentage
of their time in investigation and foraging (Wood-Gush et al., 1983). Given a facility to
manipulate an object, pigs make use of the opportunity. Pigs show ‘inquisitive exploration’
in which they learn an instrumental response for the reward of obtaining a novel object to
explore (Wood-Gush and Vestergaard, 1991).
Could insights into exploration be gained in terms of the present argument on levels
of control? In the spirit of O’Keefe and Nadel (1978), it is suggested that exploration is
triggered by a combination of external stimuli and internal representations of the world.
Based on the present model, it would appear that novelty processed by off-line controls
is a major contributor to exploration. In terms of learning within the cognitive system
(Section 3.3.2), an animal’s manipulation of its environment suggests learning and testing
of (action) → (outcome) cognitions.
One of the levels of behavioural control introduced earlier, the route VTA-N.acc.
(Section 3.4) is strongly involved in exploratory behaviour when a novel stimulus is en-
countered (Ikemoto and Panksepp, 1999; Rougé-Pont et al., 1993; Saigusa et al., 1999). A
trigger to dopaminergic activity is novelty (Schultz, 1998). Injections of amphetamine, a
DA agonist, when given in a novel environment tend to increase exploration, whereas in a
familiar environment they tend to increase stereotypy (Cooper and Dourish, 1990). By at
least some criteria, though not all, microinjection of amphetamine into the N.acc. increases
the exploratory tendency (Kelley et al., 1989). In a place-conditioning test, dopamine in the
N.acc. seems to sensitize the pull of stimuli that lead to novel objects (Bevins et al., 2002).
As the world is ‘assimilated’ into an internal (‘cognitive’) representation, so exploratory
behaviour tends to decline. This suggests a cognitive modulation of the VTA-N.acc. path-
way.
Given a choice of distinctively marked arms to get to a goal-box, typically a rat will
show alternation of choice of stimulus (whether this involves changing or repeating a motor
response), a possible indication of exploration (Montgomery, 1952). A tendency to alter-
nation is lost with damage to the hippocampus, lesioned rats exhibiting perseveration, i.e.
simply repeating the same response (Altman et al., 1973). This suggests that one role of the
hippocampus is to modulate the tendency to repetition of behaviour, based on an episodic
memory of what was most recently explored. As noted earlier, damage to the PFC–striatal
system disrupts such alternation (Dunnett and Iversen, 1981).
As the other side of the same coin, David Wood-Gush was concerned with the notion of
boredom in domestic animals and associated it with the appearance of stereotypies and other
forms of abnormal behaviour, described below (Wood-Gush and Beilharz, 1983). He noted
that the addition of sources of stimuli (e.g. toys) can reduce such maladaptive behaviour. In
terms of the present study this would amount to providing an environment that facilitates
the use of high-level cognitive control and prevents a drift into S-R control. Thus, the model
can provide additional rationale for the welfare recommendation to increase the complexity
of otherwise barren zoo environments (Stevenson, 1983).
9. Understanding stereotypies
9.1. Introduction
The model appears to be relevant to understanding the stereotypies exhibited by domestic

animals. In keeping with Fentress (1976) and Thelen (1979, 1981a), it is argued that such
stereotypies can be understood in terms of hierarchical control. It is suggested that they

are caused, at least in part, by a shift of weight to a lower level of control, i.e. a shift from
off-line to low-level, on-line, largely subcortical, controls (Dantzer, 1986; Shulman et al.,
1996; Toates, 1995, 2000). Stereotypies are by definition rhythmic and rhythm generation
is one role of lower hierarchical controls (Gallistel, 1980). As an extension of this logic,
it is argued here that such a shift of weight can occur either as a permanent function of
development or of other (transient) changes, or a combination of both. It is suggested that
such a change reflects sub-optimal information processing by higher-level systems and
thereby a shift to a lower level (Fentress, 1976; Thelen, 1979). In addition, it is argued,
there exists plasticity of lower-level controls such that repetition of a particular behaviour
has a self-strengthening (‘reinforcing’) effect (Section 3.2.2).
In some cases it appears that, as a result of experience and plasticity of neural circuits,
stereotypies come to take on the properties of powerful modal action patterns. They assume
an abnormally high candidacy for control.
9.2. Neural processes and levels of control
What are the neural bases underlying the production of stereotypies? How do these fit
a hierarchical model? Such questions draw our attention to the claim that stereotypies are
somewhat heterogeneous (Mason, 1991). Some insight might be derived from looking at
natural repetitive behaviour and its exaggeration. Thus, in rats, damage to the superior
colliculus almost abolishes the oral stereotypies of licking and gnawing triggered by am-
phetamine. However, such lesions increase locomotion in an open-field and the behaviours
of rearing and sniffing (Redgrave et al., 1980). Oral behaviours being intrinsically rhythmic
and stereotyped appear to be organized at the level of the superior colliculus but triggered
at a higher-level. They do not involve whole-body locomotion. By contrast, rearing and
locomotion involve whole-body locomotion and appear to be organized at a higher-level
with the N.acc. being involved (see earlier). The fact that a particular lesion almost abolishes
one kind of ‘stereotypy’ but enhances another, points strongly to different levels of control.
9.3. Lifting off-line controls
9.3.1. General principles

In the context of earlier development of the model (Toates, 2000), it was noted that
stereotypies arise particularly in restricted environments where there is little opportunity
for variation in behaviour. In the terms developed earlier, there is a minimal cognitive
input and, it is argued, behaviour comes under the strong control of a combination of a
few ever-present external stimuli and transition-biasing based on a restricted number of
transitions in behaviour, of the kind expressed as R2 –R3 . Which stereotypy emerges would
depend in part upon any existing links between such external stimuli as are present and
responses. Some responses would be highly probable in a given context. Other stereotypies
might emerge in a chance or arbitrary way and then dominate simply as a result of a
self-reinforcement or transition-biasing process.
In this interpretation of stereotypies, the model accords with Wemelsfelder (1993, p. 82)
in that stereotypies represent:
. . . the gradual impairment of the capacity to interact with the environment. Behaviour
acquires an increasingly rigid and mechanical character; it is determined more and more
by immediately available environmental stimuli and loses its innovative, anticipatory
nature.
It appears that stereotypies can ‘emerge from’ behaviour that naturally occurs in a given
situation, e.g. repeated attempts to escape or to gain food (Dantzer, 1986; Nevison et al.,
1999). Translating such argument to its neural basis, it is suggested that stereotypies can
appear as a result of changes in the inputs to the basal ganglia or changes intrinsic to this
structure (Shulman et al., 1996). In drug-induced stereotypies, changes in the properties
of dopaminergic neurons in the striatum underlie the emergence of stereotypy (Canales
and Graybiel, 2000). Both the candidacy of grooming and the stereotyped patterning of
sequences of grooming depend upon DA activity within the striatum (Berridge and Aldridge,
2000a,b).
Hippocampally-mediated memory is disrupted by stress and an associated excessive level
of glucocorticoids (Ohl and Fuchs, 1998, 1999). This might contribute to lifting a source
of cognitive control input and thereby bias the basal ganglia to on-line control. Stress has
disruptive effects upon hippocampal plasticity (Von Frijtag Drabbe Künzel, 2001). Monkeys
with lesions to amygdala and hippocampus exhibit increased stereotypy (Bachevalier, 1991).
Rats with damage to the cortex or hippocampus exhibit higher-levels of stereotypy, e.g. in
response to d-amphetamine injection (Devenport et al., 1981; Robbins et al., 1990). Such
results point to what is normally an inhibitory effect of hippocampal and cortical inputs on
the ascending DA projections (Robbins et al., 1990).
9.3.2. Developmental effects

Normal development involves the exertion of increasingly higher-levels of hierarchical
control and reduced levels of repetitive behaviour (Thelen, 1979). Social deprivation during
development is associated with an increased frequency of stereotyped behaviour. For ex-
ample, habitual thumb-sucking is seen in socially-deprived rhesus monkeys (Mason et al.,
1968). The fact that macaques raised alone or with an inanimate surrogate show stereotyped
body rocking appears to be a result of the absence of maternal movement. Animate objects
provide ‘contingent-stimulation’, i.e. the developing animal is able to exert control over the
social world, an example of a socially-related (response) → (outcome) cognition (Mason,
1978). Presumably development of high-level cortical controls is facilitated by stimulation
including that contingent on behaviour.
In one study on roof rats, wild-caught subjects, as opposed to laboratory-bred subjects,
did not exhibit stereotypies (Callard et al., 2000). Wild-caught voles have a low tendency to
stereotypy in the laboratory (Cooper and Nicol, 1996). A normal social development seems
to inoculate to some extent an animal against the subsequent development of stereotypies. In
chimpanzees, separation from the mother and subsequent laboratory rearing are associated
with stereotypies, whereas rearing with the mother has an inoculating effect regarding their
development (Davenport, 1979).
A study on laboratory-bred singly-housed bank voles (Clethrionomys glareolus) (Garner
and Mason, 2002) is open to interpretation in the terms of the present model. They in-
vestigated the question of whether there would be a correlation between the tendency to
stereotypy and what they termed “impaired behavioural inhibition”. Their results led them
to suggest that “caging causes striatal dysfunction”. Thus, there was a positive correlation
between (a) the magnitude of stereotypy and (b) such variables as the number of trials
needed to complete extinction of a task, which they attributed to a “striatal disinhibition
of response selection”. In the terms of the present study, evidence suggests that such brain
regions as the PFC are involved as the source of inhibition that is involved in extinction
(Section 3.3.3). A failure of such off-line control to effect action at the striatum could be
involved both in the extinction and stereotypy effects.
9.3.3. Other effects

There are various processes by means of which the weight of off-line controls could be
lowered even when the animal is adult, giving a relatively increased weight to lower-level
controls. These might be transient or more long-term effects.
Either under- or over-stimulation of dopaminergic neurons terminating in the prefrontal
cortex disrupts cognitive processes in both rodents and primates. In one experiment, dis-
ruption of such cognitive processing was indexed by the performance of a delayed al-
ternation task, in which animals tend to revert to perseverative behaviour (Zahrt et al.,
1997). This reduced efficacy of off-line control might explain why both over-stimulation and
boredom can be associated with increased stereotypy. As Zahrt et al. express it
(p. 8534):
High levels of D1 and D2 receptor stimulation during stress may synergize to take the
PFC “off-line”, thus permitting more primary cortical and subcortical structures to control
behaviour.” Arnsten (1998) notes the adaptive role of the higher-order behaviour mediated
by the PFC but suggests that:
. . . in some conditions–acute danger, for example—it might be adaptive to ‘shut down’
these complex, reflective operations and to allow more automatic, reflexive or habitual
responses dependent on the environment to control our behaviour”.
Ansten notes that the PFC is “exquisitively sensitive to its neurochemical environment,
and that catecholamines, such as dopamine and norepinephrine (NE), may have powerful
effects which switch PFC ‘on-’ or ‘off-line”’. Tasks with large working-memory demands
are most likely to be disrupted by catecholamine depletion in PFC since “. . . there is a
relatively narrow window for optimal DA receptor stimulation”.
9.4. Feedback theories
There are several variants of feedback theories of stereotypy, i.e. that, once started, they
are subsequently maintained by their consequences (Mason, 1968; Thelen, 1981b). These
theories need not be seen as necessarily competitive with the account presented here. If
an animal is in an environment that triggers stereotypies, there might be some benefit in
performing them. However, the present analysis suggests that deriving a benefit is not
a necessary condition for their emergence (cf. Dantzer, 1986). As a variety of feedback
theory, Davenport (1979) and Fox (1986, p. 64) suggest that stereotypies are a means
of providing stimulation. They reflect a kind of homeostasis: both under-stimulation and
intense stimulation are associated with stereotyped behaviour and Fox suggests that both are
associated with a deviation of stimulation from homeostasis. Spruijt et al. (2001) suggest
that stereotypies are more rewarding at times of deprivation (e.g. of food) as a result of a
general opioid-based reward sensitization.
However, there is a problem with such theories that associate stereotypies with their
consequences. The notion that they provide stimulation might explain their appearance
at times of boredom but it cannot explain their appearance at other times described by
Davenport as being strongly associated with them: just prior to feeding or after an attack.
In chimpanzees, Berkson et al. (1963) note that:
. . . they are particularly prevalent when some degree of “tension” is presumably present.
If stereotypies are a means of gaining stimulation in a barren environment, one might
expect a positive correlation between the amount of stereotypy and the exploratory re-
sponse to novel stimuli. Rather, in pigs, there is a negative correlation (Wood-Gush et al.,
1983), as would be predicted if stereotypies emerge with a shift from cognitive
control.
Turning now to humans, there is a similar logic to that just described. Tics are associated
with both boredom and stress (Bradshaw, 2001). They can be suppressed but at a price of
using mental effort. Turner (1997) discusses repetitive behaviour in the context of autism.
She notes that it is a deeply-held assumption that repetitive behaviour moves arousal nearer to
an optimal level. However, the argument is circular in that we have no independent evidence
of an optimal level of arousal towards which this behaviour causes a shift. Another problem
is that different theorists propose that individuals subject to stereotypy are either under-
or over-aroused (see Frith and Done, 1990). A process that might more parsimoniously
account for the appearance of stereotypies at both extremes of arousal is in the terms just
described.
10. Discussion
The model appears to be relevant to the study of both so-called pure and applied aspects
of animal behaviour. The evidence reviewed suggests that a closer attention to multiple
levels of control can yield considerable insight into the determinants of behaviour, normal
and abnormal.
10.1. Theoretical and philosophical issues
Are animals simple automatons, stimulus–response machines or creatures of complex

cognition, affect and possibly conscious awareness? Are they most accurately described as
passive or as active agents (Wemelsfelder, 1993)? The model proposed here suggests that
both halves of such dichotomies are partly true. Sometimes the weight of behavioural control
seems to be such that behaviour is triggered at a low-level, e.g. by particular stimuli in the
environment per se. At other times, behaviour appears to be more strongly determined by
cognitions that relate to the environment, e.g. choice based upon experience of reward in the
past or exploration based upon what was not visited in the immediate past (cf. Rumbaugh
et al., 1996). Combined control by both types of cause could provide the most broadly
applicable model. One might speculate that the higher-levels of control are most probably
associated not only with affect and feelings but such states of consciousness as can be
applied to non-humans.
The kind of model advanced here can be described as hierarchical. This is according to
the criterion that responsibility lies at different levels from the most abstract and anterior
(e.g. mediated by prefrontal cortex) to the most concrete and posterior (e.g. mediated by
brain stem and spinal cord), with each higher-level modulating that immediately below
(Bradshaw, 2001; Gallistel, 1980). Cognitive control mediated via such structures as the
PFC and hippocampus is involved in giving a level of refinement over control organized
at a lower-level. Such higher-level control appears to resist the drift to domination by
lower-level control, such drift being revealed in perseveration and stereotypy. However,
hierarchical control is not absolute. Under some conditions, physically-present powerful
stimuli can seize control in the face of higher-level controls.
Such multiple-level control appears to represent a trade-off. At one extreme, there is a
fairly automatic response that is rapid but with a relatively low resolution and appropriate
only for tasks in which there is a rather fixed connection between stimulus and a response.
At the other extreme, any reaction is relatively slow but there is a large capacity to perform
fine-grained discrimination. Where an environment is predictable, there is a gain to be had
in utilizing the lower-level of control, in terms of speed of response and ‘getting by’ with
the use of a low-level resource.
The model can be used at a philosophical level to address a broad biological prin-
ciple. Thus, it suggests that, in one important regard, ontogeny does indeed recapture
(‘recapitulate’) aspects of phylogeny (Gould, 1977), i.e. the emergence of off-line con-
trols and their increased weight relative to on-line controls is seen in both phylogeny and
ontogeny.
10.2. Welfare issues
In accordance with Wemelsfelder (1993), frustration would be associated with the thwart-
ing of high-level goal-directed behaviour. To apply her terminology, the term ‘boredom’
might be applied in a situation of transition to lower-level control, whereas something
like ‘depression’ might characterize certain states following such a shift. Logically, one
might suggest that an animal that has shifted to a low-level of control as manifest through
chronic stereotypy has a low-level of welfare (Garner and Mason, 2002). If caging re-
duces the control exerted by off-line processing, our assessment of the cognitive abilities
of an animal could be seriously undermined by observing caged subjects (cf. Würbel,
2001).
If we use the metaphor of ‘design’, it appears that complex animals that forage and
explore are designed to assimilate off-line information and to utilize it in the control of
behaviour. Good welfare might in part be indexed by the extent to which the animal is able
to exercise higher-levels of control hierarchy. If the assumptions of the model are correct,
the architects of captive environments need to take this into account for good welfare. That
is to say, a drift into undue weight being attached to lower levels of control needs to be
avoided.
10.3. Future directions
Clearly much work remains to be done in terms of the application of the model and
integration with the perspectives of other theorists. For example, it needs to be extended to
a consideration of strain differences in dopamine activation, the dimensions of attack latency
and internal versus external control of behaviour (Benus et al., 1988; Deutch and Young,
1995). It needs to be reconciled with the dichotomy of the control of behaviour described by
Vanderwolf and Robinson (1981). The model needs to be applied more closely to the role
of cortical and subcortical dopamine. For example, there are indications that cortical DA
activation is associated with the search for a coping strategy and when one is found such
activation is lowered (Deutch and Young, 1995). Potentially, this fits the notion of a shift in
weight of control. However, some results (but not all) suggest that acquisition of control over
appetitive tasks exploits DA-independent prefrontal cortical controls, as discussed earlier.
For another area calling for greater theoretical insight, the change in the neurochemical
bases of the production of stereotypies as a function of time would seem an obvious potential
candidate for explanation in terms of the model (Kennes et al., 1988). There are reports of a
reduction in stereotypies as a result of systemic injection of the DA antagonist haloperidol
(Willemse et al., 1994). This might arise from the drug targeting mainly low-level controls.
As another feature of behaviour that requires integration with the present model, it has been
argued that the frustration associated with a failure to solve a problem can lead to a kind of
automaticity or fixation of behaviour (Maier, 1949). In terms of the present argument, this
would seem to reflect some switching out of cognitive control as the power of a lower-level
control takes over.
The model might help to illuminate one of the behavioural roles of corticosteroid hor-
mones, though I would not wish to make rash statements in an area fraught with contra-
dictions. A central paradox is that whereas the level of corticosteroids is often treated as a
kind of gold-standard of stress, these hormones take on some of the properties of reward
(Piazza and Le Moal, 1997). By their synergistic action on DA neurons, they sensitize the
incentive salience pathway. Indeed, animals will learn an operant task rewarded by their
infusion. What functional significance could be attached to this? If the N.acc. serves a role
in engaging with sites of safety, it would make sense for stress to accentuate its action via
corticosteroids.
Acknowledgements
I am most grateful to Kent Berridge, Georgia Mason, Jaak Panksepp, Berry Spruijt and
Ruud Van den Bos and the referees for their comments on the manuscript.
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Cognition, Motivation, Emotion and Action A Dynamic and Vulnerable Interdependence

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Cognition, Motivation, Emotion and Action A Dynamic and Vulnerable Interdependence

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Applied Animal Behaviour Science 86 (2004) 173–204

Cognition, motivation, emotion and action: a

Keywords: Motivation; Cognition; Dopamine; Affect; Stereotypies; Welfare

E-mail address: f.toates@open.ac.uk (F. Toates).

The capacity of stimuli to trigger corresponding responses is modulated top–down by what

2.1. Basics of the model

2.2. Changing weight between levels of control

3. Identifying modes of control and associated brain mechanisms

3.2. The stimulus–response and response–response modes of control

3.2.3. Brain mechanisms

3.3. The cognitive mode of control

3.3.2. Learning and cognition

3.3.3. Brain mechanisms

3.4. The ventral tegmental area—nucleus accumbens pathway

3.4.2. Aversive situations

4. Competition between levels of control

4.2. Brain mechanisms

4.3. Some examples of competition for control

4.3.2. Activity levels

VTA-N.acc. route (‘incentive motivation pathway’) according to context and particular

4.3.4. The ‘misbehaviour’ of organisms

5. Affect and emotion

5.3.2. How emotions arise

5.3.3. What emotion does

6.2. Deprivation effects

8. Exploration and boredom

The model appears to be relevant to understanding the stereotypies exhibited by domestic

stereotypies can be understood in terms of hierarchical control. It is suggested that they

9.2. Neural processes and levels of control

9.3. Lifting off-line controls

9.3.1. General principles

9.3.2. Developmental effects

9.3.3. Other effects

9.4. Feedback theories

10.1. Theoretical and philosophical issues

Are animals simple automatons, stimulus–response machines or creatures of complex

10.2. Welfare issues

10.3. Future directions

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