A Specialized Area in Limbic Cortex for Fast Analysis of Peripheral Vision

Abstract

In primates, prostriata is a small area located between the primary visual cortex (V1) and the hippocampal formation. Prostriata sends connections to multisensory and high-order association areas in the temporal, parietal, cingulate, orbitofrontal, and frontopolar cortices. It is characterized by a relatively simple histological organization, alluding to an early origin in mammalian evolution. Here we show that prostriata neurons in marmoset monkeys exhibit a unique combination of response properties, suggesting a new pathway for rapid distribution of visual information in parallel with the traditionally recognized dorsal and ventral streams. Whereas the location and known connections of prostriata suggest a high-level association area, its response properties are unexpectedly simple, resembling those found in early stages of the visual processing: neurons have robust, nonadapting responses to simple stimuli, with latencies comparable to those found in V1, and are broadly tuned to stimulus orientation and spatiotemporal frequency. However, their receptive fields are enormous and form a unique topographic map that emphasizes the far periphery of the visual field. These results suggest a specialized circuit through which stimuli in peripheral vision can bypass the elaborate hierarchy of extrastriate visual areas and rapidly elicit coordinated motor and cognitive responses across multiple brain systems.

Peripheral sounds rapidly activate visual cortex: evidence from electrocorticography

“…Electrodes within primary visual cortex were selected for analyses based on their anatomic location within the calcarine sulcus. Studies examining the cytoarchitectonically delineated border of V1 in humans show that in a small subset of individuals secondary visual cortex and visual region prostriata expand into the anterior calcarine sulcus (Amunts et al 2000;Yu et al 2012), introducing the possibility that the recorded activity in our patients included neural responses from these regions as well as from primary visual cortex.…”

Representation of central and peripheral vision in the primate cerebral cortex: Insights from studies of the marmoset brain

“…However, prostriata neurons also have features that are considered signatures of higher-level areas, such as large receptive fields and broad connectivity to non-visual areas, including the auditory cortex (Rockland and Ojima, 2003;Falchier et al, 2010), motor areas in the cingulate cortex (Morecraft et al, 2000(Morecraft et al, , 2004, association areas in the superior temporal cortex (Seltzer and Pandya, 1994) and posterior parietal cortex (Rockland and Ojima, 2003), parahippocampal cortex (Blatt et al, 2003), and frontal areas (Barbas, 1988;Cavada et al, 2000;Burman et al, 2011). As suggested by Yu et al (2012), prostriata might be part of a pathway that allows information of the far peripheral visual field to bypass the elaborate hierarchy of visual processing and rapidly engage a wide range of cortical functions.…”

“…Motivated by the results of the tracer injection study of Palmer and Rosa (2006), we revisited the issue of visual responses in prostriata in anaesthetized marmosets (Yu et al, 2012), using a panoramic display system that was optimized for stimulating the peripheral visual field . Immediately rostral to the sector of V1 that represents the outer boundary of the field of vision, we encountered robust responses to visual stimulation.…”

“…Although the first basic characterizations of its neuronal response properties have been reported (Yu et al, 2012), much work is still required to understand its functions. Complex stimuli with emotional contents, or scenes with environmental cues are likely to prove fruitful.…”

The cortical motor system of the marmoset monkey (Callithrix jacchus)

“…Functions attributed to these caudal areas are biased toward visuospatial analyses for orientation and navigation, memory, and attention (Vogt and Laureys, 2005;Vann et al, 2009;Kravitz et al, 2013). At least some of these functions might be accomplished via the oculomotor system, and posteromedial areas exhibit eye-movement-or eyeand-hand-related activity (Olson et al, 1996;Ferraina et al, 1997;Thier and Andersen, 1998;Dean et al, 2004), and connections with visual and oculomotor fields (Cavada and Goldman-Rakic, 1989a,b;Leichnetz, 2001;Morecraft et al, 2004;Passarelli et al, 2013), including representations of the peripheral visual field (Rosa and Schmid, 1995;Yu et al, 2012). Although many of the functions for this system have been described in rather broad anatomical terms in macaques (Cavanna and Trimble, 2006;Vann et al, 2009), the main point here is that robust posteromedial connections characterize macaque and marmoset 6DR cortex, suggesting a highly conserved pathway among primates.…”