ReviewReward expectation alters learning and memory: The impact of the amygdala on appetitive-driven behaviors
Section snippets
Pavlovian associations produce specific reward expectancies that can modulate instrumental behavior
Expectations of reward can have powerful effects on learning and performance. Learning to anticipate a reward can occur by associating a discrete stimulus (S–O; Pavlovian conditioning) and/or an action (R–O; instrumental conditioning) with an outcome (see Fig. 1A). A predictive cue such as a conditioned stimulus (CS) or discriminative stimulus (SD) can enter into associations with either the general motivational properties of the reward or the sensory specific properties of reward (see [23],
Reward expectancies produced by the DOP can change behavioral success after brain damage
Our laboratory [98], [95], [94], [84], [72] proposed that the DOP allows subjects to use reward expectancies to solve the task and this cognitive process activates different brain regions compared to when a subject must rely on retrospective recall of information (as must be done under NOP conditions) to solve a task. The reliance on reward-related processes activates a memory system that is different, structurally and associatively, from the system commonly used to solve conditional
Functional evidence for the role of the amygdala in Pavlovian associative processes
There is an accumulation of evidence from a number of studies that the amygdala is critical for expectancy of both aversive and appetitive outcomes. In all species examined, the amygdala plays an important role in Pavlovian conditioning and significant progress has been made in understanding the neural mechanisms of Pavlovian-conditioned fear. For example, functional neuroimaging studies indicate an increased hemodynamic response in the human amygdala during presentation of CSs such as faces,
Specific conditions evoke the BLA in the development and maintenance of reward expectancies
There is evidence from a number of procedures that the amydala is critical for the development of reward expectancies. As describe in detail below, lesions of the BLA produce deficits in Pavlovian second-order conditioning, the reward specific effects of reinforcer devaluation, the differential outcomes effect, and reward-specific Pavlovian-to-instrumental transfer (PIT; [11], [36], [84]). However, lesions to the BLA do not affect acquisition of approach or orientation behaviors elicited by a
Summary
Reward expectancies can be evoked to direct behavior under a range of circumstances. Environmental conditions set the stage for the type of associative relationships that an organism will form between stimuli, responses and outcomes. Data suggest that several interconnected brain structures – the basolateral amygdala (BLA), the orbitofrontal cortex (OFC), and the nucleus accumbens (NA) are part of the neural circuitry that is integral for cues that predict features of reward and goal-directed
References (119)
- et al.
Goal-directed instrumental action: contingency and incentive learning and their cortical substrates
Neuropharmacology
(1998) - et al.
Parallel incentive processing: an integrated view of amygdala function
Trends Neurosci
(2006) - et al.
Infralimbic cortex activation increases c-Fos expression in intercalated neurons of the amygdala
Neurosci
(2005) - et al.
Classical fear conditioning in functional neuroimaging
Curr Opin Neurobiol
(2000) - et al.
Brain systems mediating aversive conditioning: an event-related fMRI study
Neuron
(1998) - et al.
Induction of the c-fos proto-oncogene in rat amygdala during unconditioned and conditioned fear
Brain Res
(1991) - et al.
Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex
Neurosci Biobehav Rev
(2002) - et al.
Locomotor sensitization to cocaine is associated with increased Fos expression in the accumbens, but not in the caudate
Behav Brain Res
(2002) - et al.
Spatial learning deficits in old rats: a model for memory decline in the aged
Neurobiol Aging
(1988) - et al.
Sensitized Fos expression in subterritories of the rat medial prefrontal cortex and nucleus accumbens following amphetamine sensitization as revealed by stereology
Brain Res
(2002)
Cardiovascular responses elicited by stimulation of neurons in the central amygdaloid nucleus in awake but not anesthetized rats resemble conditioned emotional responses
Brain Res
Cardiovascular responses elicited by electrical stimulation of the amygdala central nucleus in the rabbit
Brain Res
Pavlovian CS effects upon instrumental choice behavior are reinforcer specific
Learn Motiv
Thiamine deficiency in rats produces cognitive and memory deficits on spatial tasks that correlate with tissue loss in diencephalon, cortex and white matter
Behav Brain Res
Overlapping projections to the amygdala and striatum from auditory processing areas of the thalamus and cortex
Neurosci Lett
Thiamine deficiency depletes cortical norepinephrine and impairs learning processes in the rat
Brain Res
Synaptic mechanisms of associative memory in the amygdala
Neuron
Corticoamygdaloid and corticocortical projections of the rat temporal cortex: a Phaseolus vulgaris leucoagglutinin study
Neurosci
Cortical pathways to the mammalian amygdala
Prog Neurobiol
Production of the Fos protein after contextual fear conditioning of C57BL/6N mice
Brain Res
Effects of altering outcome expectancies on Pigeons’ delayed conditional discrimination performance
Learn Motiv
Organization of intra-amygdaloid circuitries in the rat: an emerging framework for understanding functions of the amygdala
Trends Neurosci
Neurons in rat medial prefrontal cortex show anticipatory rate changes to predictable differential rewards in a spatial memory task
Behav Brain Res
Fear conditioning enhances different temporal components of tone-evoked spike trains in auditory cortex and lateral amygdala
Neuron
Fear conditioning enhances short-latency auditory responses of lateral amygdala neurons: parallel recordings in the freely behaving rat
Neuron
The role of the GABAA agonist muscimol on memory performance: Reward contingencies determine the nature of the deficit
Neurobiol Learn Mem
Molecular mechanisms underlying emotional learning and memory in the lateral amygdala
Neuron
Cue valence representation studied by Fos immunocytochemistry after acquisition of a discrimination learning task
Brain Res Bull
Bidirectional synaptic plasticity in intercalated amygdala neurons and the extinction of conditioned fear responses
Neurosci
The effect of hippocampal lesions on learning, memory and reward expectancies
Neurobiol Learn Mem
Rats exposed to acute pyrithiamine-induced thiamine deficiency are more sensitive to the amnestic effects of scopolamine and MK-801: examination of working memory, response selection and reinforcement contingencies
Behav Brain Res
Neuronal activity in monkey striatum related to the expectation of predictable environmental events
J Neurophysiol
The effect of lesions of the basolateral amygdala on instrumental conditioning
J Neurosci
Behavioral and neurophysiological examples of functional sparing in senescent rats
Canadian J Psychology
The amygdala and reward
Nat Rev Neurosci
Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans
Science
Conditioned fear-induced changes in behavior and in the expression of the immediate early gene c-fos: with and without diazepam pretreatment
J Neurosci
Synaptic plasticity in the lateral amygdala: a cellular hypothesis of fear conditioning
Learn Mem
Lesions of the Basolateral Amygdala Disrupt Selective Aspects of Reinforcer Representation in Rats
J Neurosci
Conditioned reinforcement can be mediated by either outcome-specific or general affective
Frontiers in Integrative Neurosci
Functional MRI of human amygdala activity during Pavlovian fear conditioning: stimulus processing versus response expression
Behav Neurosci
Differential fear conditioning induces reciprocal changes in the sensory responses of lateral amygdala neurons to the CS(+) and CS(-)
Learn Mem
Double dissociation of basolateral and central amygdala lesions on the general and outcome-specific forms of pavlovian-instrumental transfer
J Neurosci
The role of the nucleus accumbens in instrumental conditioning: evidence of a functional dissociation between accumbens core and shell
J Neurosci
Olfactory neuronal responses in the primate orbitofrontal cortex: analysis in an olfactory discrimination task
J Neurophysiol
The role of the orbitofrontal cortex in sensory-specific encoding of associations in Pavlovian and instrumental conditioning
Ann NY Acad Sci
Enhancement of matching acquisition by differential comparison – outcome associations
J Exp Psych: Animal Behav Processes
Cells in the posterior thalamus project to both amygdala and temporal cortex: a quantitative retrograde double-labeling study in the rat
J Comp Neurol
Organization of projections to the lateral amygdala from auditory and visual areas of the thalamus in the rat
J Comp Neurol
Delay-dependent short-term memory deficits in aged rats
Psychophamacology
Cited by (50)
Investigation of donkeys learning capabilities through an operant conditioning
2022, Applied Animal Behaviour ScienceImplicit outcomes expectancies shape memory process: Electrophysiological evidence
2020, Biological PsychologyCitation Excerpt :These findings extend the results of the study by Carmona et al. (2020) and provide evidence for a greater efficiency across most of the components analyzed with the DOP. In sum, the neuronal electrical patterns explored in this study revealed that different mechanisms were activated depending on the outcomes condition, which is consistent with previous studies (Carmona et al., 2019; Carmona et al., 2020; Mok, 2012; Mok, Thomas, Lungu, & Overmier, 2009) as well as with the two memory system model proposed by Savage and colleagues (e.g., Savage & Ramos, 2009). To our knowledge, the present findings provide, for the first time, electrophysiological evidence of implicit prospective processes involved in the DOP, which result in an improved visual recognition memory.
Electrophysiological correlates of the differential outcomes effect in visual short-term memory
2020, International Journal of PsychophysiologyDoes the implicit outcomes expectancies shape learning and memory processes?
2019, CognitionCitation Excerpt :One relevant question we might ask is whether being aware of the specific consequences of our actions is a necessary condition for them to have beneficial effects in cognition (as demonstrated by the DOP effect). The two-memory systems theory (e.g., Savage & Ramos, 2009) would claim this not be the case, because expectancies of the specific outcomes are implicitly formed via classical conditioning associations (i.e., sample stimulus-outcome). After several pairings, the presentation of the sample stimulus would activate the representation of its own and unique outcome and this can be used to make the correct choice.