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. 2006 Feb 16;439(7078):865-70.
doi: 10.1038/nature04490.

The primate amygdala represents the positive and negative value of visual stimuli during learning

Joseph J Paton  1 , Marina A Belova, Sara E Morrison, C Daniel Salzman
Affiliations

The primate amygdala represents the positive and negative value of visual stimuli during learning

Joseph J Paton et al. Nature. .

Abstract

Visual stimuli can acquire positive or negative value through their association with rewards and punishments, a process called reinforcement learning. Although we now know a great deal about how the brain analyses visual information, we know little about how visual representations become linked with values. To study this process, we turned to the amygdala, a brain structure implicated in reinforcement learning. We recorded the activity of individual amygdala neurons in monkeys while abstract images acquired either positive or negative value through conditioning. After monkeys had learned the initial associations, we reversed image value assignments. We examined neural responses in relation to these reversals in order to estimate the relative contribution to neural activity of the sensory properties of images and their conditioned values. Here we show that changes in the values of images modulate neural activity, and that this modulation occurs rapidly enough to account for, and correlates with, monkeys' learning. Furthermore, distinct populations of neurons encode the positive and negative values of visual stimuli. Behavioural and physiological responses to visual stimuli may therefore be based in part on the plastic representation of value provided by the amygdala.

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Figures

Figure 1
Figure 1. Task and brain MRI
a, Sequence of events for the three trial types. Top and bottom squares, image values reverse. Middle square, image always non-reinforced. b, Coronal MRI acquired with a two-dimensional (2D) spoiled gradient recalled acquisition (SPGR) sequence in monkey V, showing the artefact from a tungsten microelectrode dorsal to the amygdala (outlined in white). c–f, Coronal MRI with 2D inversion recovery (IR) sequence (c, arrows point to the electrode). Magnified images show the probable border of the lateral nucleus (arrow in d) and recording site locations (slice in f is immediately posterior to e). We collapsed recording sites spanning 2 mm in the anterior–posterior dimension onto each image slice, in many cases resulting in the superposition of multiple cells with different properties (see key above f for symbols denoting properties; ‘ + ’ denotes positive value-coding, ‘ − ’ denotes negative value-coding, and ‘no’ symbol indicates no value-coding). Recording sites from monkey P occurred in an overlapping region of the amygdala.
Figure 2
Figure 2. Behaviour and neural activity from a single amygdala neuron during learning
a, b, Cumulative (curves) and trial-by-trial (tick marks) measures of licking (red) and blinking (blue), plotted as a function of trial number for images 1 and 2. Black dots indicate change points. Vertical green lines indicate value reversals. c–f, Rasters and peri-stimulus time histograms (PSTHs), truncated at US delivery, for the amygdala cell recorded during the same experiment. Each row of dots represents the timing of action potentials during one trial. PSTHs sum activity across trials and were smoothed by taking a 10-ms moving average of activity. Blue ticks indicate fixation point onset. Red ticks indicate visual stimulus onset/offset. g, h, Spike count and cumulative spike count during the trace interval, plotted as a function of trial number for images 1 and 2. Red dots indicate change points.
Figure 3
Figure 3. Amygdala neurons encode the positive and negative value of visual stimuli
a, b, Image identity coding index (II_CI) plotted against image value coding index (IV_CI) for the visual stimulus (VS) and trace intervals. Green, blue and red dots, P < 0.05 for II_CI, IV_CI or both indices, respectively (two-way ANOVA). Yellow dots, not significant. Inset histograms show II_CI subtracted from IV_CI for non-yellow data points. See Supplementary Fig. 9. c, Encoding of positive and negative value shown by ROC analysis. d, Development of value signals as a function of time. Each row in the colour map represents value coding for a neuron during presentation of a single image, with positive and negative cell rows sorted in opposite order according to the first post-visual-stimulus data point significantly different from 0.5 (P < 0.05, permutation test). White curves show mean ROC values across the positive- and negative-coding populations. Time 0 is the start of the bin spanning from 0–99 ms after visual stimulus onset.
Figure 4
Figure 4. The relationship between changes in neural activity and behavioural responses
a, b, Onset of changes in neural activity plotted against the onset of changes in licking or blinking for visual stimulus (VS) and trace interval activity. Histograms show the difference between neural and behavioural change points. Blue, data and regression lines for monkey V; red, data and regression lines for monkey P. c, Average normalized neural activity and behavioural responses plotted as a function of trial number relative to the reversal in image value. Shaded regions indicate 95% prediction intervals for best-fit Weibull functions. d, Similar representation as in c, applied to the non-reinforced images. Shaded regions show s.e.m. of data points.
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