Face-selective neurons maintain consistent visual responses across months

Abstract

Face perception in both humans and monkeys is thought to depend on neurons clustered in discrete, specialized brain regions. Because primates are frequently called upon to recognize and remember new individuals, the neuronal representation of faces in the brain might be expected to change over time. The functional properties of neurons in behaving animals are typically assessed over time periods ranging from minutes to hours, which amounts to a snapshot compared to a lifespan of a neuron. It therefore remains unclear how neuronal properties observed on a given day predict that same neuron's activity months or years later. Here we show that the macaque inferotemporal cortex contains face-selective cells that show virtually no change in their patterns of visual responses over time periods as long as one year. Using chronically implanted microwire electrodes guided by functional MRI targeting, we obtained distinct profiles of selectivity for face and nonface stimuli that served as fingerprints for individual neurons in the anterior fundus (AF) face patch within the superior temporal sulcus. Longitudinal tracking over a series of daily recording sessions revealed that face-selective neurons maintain consistent visual response profiles across months-long time spans despite the influence of ongoing daily experience. We propose that neurons in the AF face patch are specialized for aspects of face perception that demand stability as opposed to plasticity.vision | fMRI | physiology M any biological systems perform in a stable manner over time. The consistent behavior that is evident at the global level of the organism can persist despite continuous change in the system's component parts. A cup of coffee, for instance, tastes the same today as it did one year ago, despite the fact that the receptors in our taste buds are replaced every two weeks (1). In addition to the continuous replacement of individual cells, the protein constituents of cells likewise undergo nearly continuous turnover (2). What happens in the central nervous system? Because the lifespan of most neurons in the brain approaches that of the organism (3), it is conceivable that the population of faceselective cells that fire today when you see your mother, for instance, is identical to the population that fired under the same circumstances 10 years ago. However, in the absence of direct evidence, there is no reason to assume that this is the case, or more generally that stable network performance implies stable units. And indeed, both theoretical (4) and experimental results from motor cortex (5, 6) demonstrate that a network composed of unstable units may nonetheless exhibit stable performance. Recent recordings from the mouse hippocampus showed that reliable location signaling is driven largely by neurons that gradually enter and leave the population of functionally active place cells over the course of several days (7). In that study, only 15% of longitudinally monitored neurons were found to retain the same place fields in two sessions that were separ...

Contrasting Specializations for Facial Motion within the Macaque Face-Processing System

“…This preference for natural facial motion suggests that cells in MD and AF, beyond selectivity for static facial form (Figure 2D; see [24]), also exhibit selectivity for the kinematics of naturally moving faces. Some neurons in these patches may fire only in response to a specific sequence of poses, a mechanism that has been proposed for the neural coding of biological motion [25, 26].…”

Variance and invariance of neuronal long-term representations

“…[17,18]). Only recent years have seen a prominent increase in the number of mostly imaging studies addressing the stability and plasticity of neuronal representations in the visual system [15,19,35,36,38,41,43,44,46], barrel cortex [14,29,39,47,60] and auditory cortex [42]. …”

“…All these factors are likely to directly affect the assessment of neuronal variability. Furthermore, longitudinal recordings of cellular activity have been performed using a plethora of different experimental paradigms in multiple preparations—from in vitro recordings in dissociated cultures [58,59] to in vivo recordings in primary and higher sensory areas [14,15,18,19,29,35,36,38,39,41–44,46,47,49,60], motor areas [22,27,37,48,55,61–65], striatum [22] and hippocampus [28,40,45,52,66–69]. Comparing the variability of neuronal feature selectively therefore is challenging—nevertheless, we would first like to provide an update on long-term neuronal variability assessments (for a previous in-depth review see [16]; for a review on short-term trial-to-trial variabiliy see [70]).…”

Managing complexity: from visual perception to sustainable transitions—contributions of Brunswik’s Theory of Probabilistic Functionalism

“…Obviously, there are highly specialized cells in the inferior visual cortex for specific and important highly complex perception such as facial recognition. This may be illustrated by the ''grandmother cell'' hypothesis (Gross 2002;McMahon et al 2014). There is evidence that specific cells may reliably identify certain faces in the short term and after a long time.…”