The primate amygdala and reinforcement: A dissociation between rule-based and associatively-mediated memory revealed in neuronal activity

doi:10.1016/j.neuroscience.2005.03.022

Neuroscience

Volume 133, Issue 4, 2005, Pages 1061-1072

https://doi.org/10.1016/j.neuroscience.2005.03.022 Get rights and content

Abstract

To investigate the role of the primate amygdala in stimulus-reinforcement association learning, the activity of single amygdala neurons was recorded in macaques during two memory tasks. In a visual discrimination task, a population of neurons (17/659) was analyzed which responded differentially to a visual stimulus which always indicated that the primary reinforcer fruit juice could be obtain if the monkey licked, and a different visual stimulus that indicated that the primary reinforcer aversive saline would be obtained if the monkey licked. Most (16/17) of these neurons responded more to the reward-related than the aversive visual stimulus. In a recognition memory task, the majority (12/14 analyzed) of these neurons responded equally well to the trial unique stimuli when they were shown as novel and the monkey had to not lick in order to avoid saline, and when they were shown a second time as familiar and the monkey used the rule that if he licked, fruit juice would be obtained. The responses of these amygdala neurons thus reflect the direct associations of stimuli with reinforcement, but do not reflect the reward value of the stimuli when this must be assessed based on a rule (in the recognition memory task, that a stimulus will be punished the first time it is shown, and rewarded the second). This finding also shows that these amygdala neurons respond to relatively novel stimuli in the same way as they do to stimuli that have become rewarding by stimulus-reinforcement association learning. This provides a neural basis for relatively novel stimuli to be treated as rewarding, and approached.

Section snippets

Subjects, stimulus presentation, behavioral responses, and reinforcement

Two rhesus monkeys (Macaca mulatta) were used in this study and were trained on a visual discrimination task with stimuli that were always rewarded or punished, and on a recognition memory task. They performed these tasks with many hundreds of trials per day, five days a week, for periods of up to 14 months. When sitting in the primate chair the monkeys’ view of the laboratory was limited to a circular aperture in an enclosure that surrounded the chair. Head support and the enclosure ensured

Results

A total of 659 neurons in 92 electrode penetrations were recorded in three hemispheres of two monkeys. The classification of all recorded neurons is found in Table 1. [The ten neurons in row 3 of Table 1 with responses only to novel stimuli have been described by Wilson and Rolls (1993)]. Of the 659 neurons shown in Table 1, for 17 neurons it was possible to show that they had visual responses, discriminated between the reward- and punishment-associated stimuli in the Go/NoGo visual

Amygdala neurons and associations between visual stimuli and primary reinforcers

The present results show the following. First, a population of amygdala neurons responds differentially to rewarding and aversive stimuli in a visual discrimination task with which the monkeys have had many thousands of trials of experience. This population of neurons typically responds more to the S+ than the S−. This confirms the finding of Sanghera et al. (1979), and the data of Nishijo et al. (1988) are consistent with this. The fact that there are many amygdala neurons that respond more to

Acknowledgments

This research was supported by a Medical Research Council Programme Grant to E. T. Rolls.

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¹: Present address: Kunming Institute of Zoology, The Chinese Academy of Sciences, 32 Jiaochang Donglu, Kunming, Yunnan 650223, P.R. China. E-mail address: [email protected] (F. A. W. Wilson).

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Systems neuroscienceThe primate amygdala and reinforcement: A dissociation between rule-based and associatively-mediated memory revealed in neuronal activity

Abstract

Section snippets

Subjects, stimulus presentation, behavioral responses, and reinforcement

Results

Amygdala neurons and associations between visual stimuli and primary reinforcers

Acknowledgments

Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala

Nature

A description of intra-amygdaloid connections in old world monkeys

Exp Brain Res

Stereotaxic surgery under X-ray guidance in the rhesus monkey, with special reference to the amygdala

Exp Brain Res

Syndrome produced by lesions of the amygdala in monkeys (Macaca mulatta)

J Comp Physiol Psychol

Multiple measures of the orienting reaction and their dissociation after amygdalectomy in monkeys

Exp Neurol

The amygdala and reward

Nat Rev Neurosci

Computational handbook of statistics

Attention and working memorya dynamical model of neuronal activity in the prefrontal cortex

Eur J Neurosci

Synaptic and spiking dynamics underlying reward reversal in orbitofrontal cortex

Cereb Cortex

Allocentric and egocentric spatial information processing in the hippocampal formation of the behaving primate

Psychobiology

Monkeys’ recognition memory for complex pictures and the effect of fornix transection

Quart J Exp Psychol

The neurobiology of visual-saccadic decision making

Annu Rev Neurosci

Temporal neocortical afferent connections to the amygdala in the rhesus monkey

Brain Res

Partial Kluver-Bucy syndrome produced by destroying temporal neocortex or amygdala

Brain Res

‘Interest’ and ‘pleasure’two determinants of a monkey’s visual preferences

Perception

Amygdalofugal and amygdalopetal connections with modality-specific visual cortical areas in macaques (Macaca fuscata, M. mulatta, and M. fascicularis)

J Comp Neurol

Limbic lesions and the problem of stimulus-reinforcement associations

Exp Neurol

The primate amygdalaneuronal representations of the viscosity, fat texture, grittiness and taste of foods

Neuroscience

Neurons in the amygdala of the monkey with responses selective for faces

Behav Brain Res

Excitotoxic lesions of the amygdala fail to produce impairment in visual learning for auditory secondary reinforcement but interfere with reinforcer devaluation effects in rhesus monkeys

J Neurosci

Multiple functional contributions of the amygdala in the monkey

Modulation during learning of the responses of neurones in the lateral hypothalamus to the sight of food

Exp Neurol

Anterior rhinal cortex and amygdaladissociation of their contributions to memory and food preference in rhesus monkeys

Behav Neurosci

Feeding-related activity of glucose- and morphine-sensitive neurons in the monkey amygdala

Brain Res

Single neuron responses in amygdala of alert monkey during complex sensory stimulation with affective significance

J Neurosci

The representation of pleasant and aversive taste in the human brain

J Neurophysiol

Electrophysiological characteristics of amygdaloid central nucleus neurons during Pavlovian fear conditioning in the rabbit

Behav Brain Res

Systems neuroscience
The primate amygdala and reinforcement: A dissociation between rule-based and associatively-mediated memory revealed in neuronal activity