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Encoding of Stimulus Probability in Macaque Inferior Temporal Cortex.

ABSTRACT: Optimal perceptual decisions require sensory signals to be combined with prior information about stimulus probability. Although several theories propose that probabilistic information about stimulus occurrence is encoded in sensory cortex, evidence from neuronal recordings has not yet fully supported this view. We recorded activity from single neurons in inferior temporal cortex (IT) while monkeys performed a task that involved discriminating degraded images of faces and fruit. The relative probability of the cue being a face versus a fruit was manipulated by a latent variable that was not revealed to the monkeys and that changed unpredictably over the course of each recording session. In addition to responding to stimulus identity (face or fruit), population responses in IT encoded the long-term stimulus probability of whether a face or a fruit stimulus was more likely to occur. Face-responsive neurons showed reduced firing rates to expected faces, an effect consistent with "expectation suppression," but expected stimuli were decoded from multivariate population signals with greater accuracy. These findings support "predictive coding" theories, whereby neural signals in the mammalian visual system actively encode and update predictions about the local sensory environment.

SUBMITTER: Bell AH

PROVIDER: S-EPMC5021632 | biostudies-literature | 2016 Sep

REPOSITORIES: biostudies-literature

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Encoding of Stimulus Probability in Macaque Inferior Temporal Cortex.

Bell Andrew H AH Summerfield Christopher C Morin Elyse L EL Malecek Nicholas J NJ Ungerleider Leslie G LG

Current biology : CB 20160811 17

Optimal perceptual decisions require sensory signals to be combined with prior information about stimulus probability. Although several theories propose that probabilistic information about stimulus occurrence is encoded in sensory cortex, evidence from neuronal recordings has not yet fully supported this view. We recorded activity from single neurons in inferior temporal cortex (IT) while monkeys performed a task that involved discriminating degraded images of faces and fruit. The relative prob ...[more]

PMID: 27524483

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Project description:Primates have specialized domains in inferior temporal (IT) cortex that are responsive to particular image categories. Though IT traditionally has been regarded as lacking retinotopy, several recent studies in monkeys have shown that retinotopic maps extend to face patches along the lower bank of the superior temporal sulcus (STS) and neighboring regions of IT cortex. Here, we used fMRI to map the retinotopic organization of medial ventral temporal cortex in four monkeys (2 male and 2 female). We confirm the presence of visual field maps within and around the lower bank of the STS and extend these prior findings to scene-selective cortex in the ventral-most regions of IT. Within the occipitotemporal sulcus (OTS), we identified two retinotopic areas, OTS1 and OTS2. The polar angle representation of OTS2 was a mirror reversal of the OTS1 representation. These regions contained representations of the contralateral periphery and were selectively active for scene versus face, body, or object images. The extent of this retinotopy parallels that in humans and shows that the organization of the scene network is preserved across primate species. In addition retinotopic maps were identified in dorsal extrastriate, posterior parietal, and frontal cortex as well as the thalamus, including both the lateral geniculate nucleus and pulvinar. Together, it appears that most, if not all, of the macaque visual system contains organized representations of visual space.SIGNIFICANCE STATEMENT Primates have specialized domains in inferior temporal (IT) cortex that are responsive to particular image categories. Though retinotopic maps are considered a fundamental organizing principle of posterior visual cortex, IT traditionally has been regarded as lacking retinotopy. Recent imaging studies have demonstrated the presence of several visual field maps within the lateral IT. Using neuroimaging, we found multiple representations of visual space within ventral IT cortex of macaques that included scene-selective cortex. Scene domains were biased toward the peripheral visual field. These data demonstrate the prevalence of visual field maps throughout the primate visual system, including late stages in the ventral visual hierarchy, and support the idea that domains representing different categories are biased toward different parts of the visual field.

Project description:Orbitofrontal cortex (OFC), medial frontal cortex (MFC), and amygdala mediate stimulus-reward learning, but the mechanisms through which they interact are unclear. Here, we investigated how neurons in macaque OFC and MFC signaled rewards and the stimuli that predicted them during learning with and without amygdala input. Macaques performed a task that required them to evaluate two stimuli and then choose one to receive the reward associated with that option. Four main findings emerged. First, amygdala lesions slowed the acquisition and use of stimulus-reward associations. Further analyses indicated that this impairment was due, at least in part, to ineffective use of negative feedback to guide subsequent decisions. Second, the activity of neurons in OFC and MFC rapidly evolved to encode the amount of reward associated with each stimulus. Third, amygdalectomy reduced encoding of stimulus-reward associations during the evaluation of different stimuli. Reward encoding of anticipated and received reward after choices were made was not altered. Fourth, amygdala lesions led to an increase in the proportion of neurons in MFC, but not OFC, that encoded the instrumental response that monkeys made on each trial. These correlated changes in behavior and neural activity after amygdala lesions strongly suggest that the amygdala contributes to the ability to learn stimulus-reward associations rapidly by shaping encoding within OFC and MFC.SIGNIFICANCE STATEMENT Altered functional interactions among orbital frontal cortex (OFC), medial frontal cortex (MFC), and amygdala are thought to underlie several psychiatric conditions, many related to reward learning. Here, we investigated the causal contribution of the amygdala to the development of neuronal activity in macaque OFC and MFC related to rewards and the stimuli that predict them during learning. Without amygdala inputs, neurons in both OFC and MFC showed decreased encoding of stimulus-reward associations. MFC also showed increased encoding of the instrumental responses that monkeys made on each trial. Behaviorally, changes in neural activity were accompanied by slower stimulus-reward learning. The findings suggest that interactions among amygdala, OFC, and MFC contribute to learning about stimuli that predict rewards.

Dataset Information

Encoding of Stimulus Probability in Macaque Inferior Temporal Cortex.

Publications

Encoding of Stimulus Probability in Macaque Inferior Temporal Cortex.

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