Heterogeneity in the Responses of Adjacent Neurons to Natural Stimuli in Cat Striate Cortex

Abstract

When presented with simple stimuli like bars and gratings, adjacent neurons in striate cortex exhibit shared selectivity for multiple stimulus dimensions, such as orientation, direction, and spatial frequency. This has led to the idea that local averaging of neuronal responses provides a more reliable representation of stimulus properties. However, when stimulated with complex, time-varying natural scenes (i.e., movies), striate neurons exhibit highly sparse responses. This raises the question of how much response heterogeneity the local population exhibits when stimulated with movies, and how it varies with separation distance between cells. We investigated this question by simultaneously recording the responses of groups of neurons in cat striate cortex to the repeated presentation of movies using silicon probes in a multi-tetrode configuration. We found, first, that the responses of striate neurons to movies are brief (tens of milliseconds), decorrelated, and exhibit high population sparseness. Second, we found that adjacent neurons differed significantly in their peak firing rates even when they responded to the same frames of a movie. Third, pairs of adjacent neurons recorded on the same tetrodes exhibited as much heterogeneity in their responses as pairs recorded by different tetrodes. These findings demonstrate that complex natural scenes evoke highly heterogeneous responses within local populations, suggesting that response redundancy in a cortical column is substantially lower than previously thought.

A general rule for sensory cue summation: evidence from photographic, musical, phonetic and cross-modal stimuli

“…We still have an incomplete understanding of the magnitudes of typical correlation coefficients between neural responses, especially when the systems are studied with natural stimuli [38]. There have been many studies, particularly in various cortical areas of the visual system (e.g.…”

Spatial and temporal jitter distort estimated functional properties of visual sensory neurons

“…Characteristics of receptive field dynamics (DeAngelis et al 1993;Malone et al 2007;Ringach et al 1997) are also affected by the reported findings, especially when considering the evolution of frequency selectivity (Malone et al 2007). Additionally, observed heterogeneity and distribution of receptive field sizes and types (Gawne et al 1996;Maldonado and Gray 1996;Yen et al 2007) may be even larger than reported.…”

“…91-3207 (National Institutes of Heath, Bethesda, MD, 1991). A detailed description of the surgical and recording techniques can be found in Yen et al (2007).…”

Mapping of contextual modulation in the population response of primary visual cortex

“…The dominance of inhibitory influences in the population is usually interpreted as an effect of the retinotopic surround (Angelucci et al 2002), but could equally well be explained from the more general principle of sparseness of neuronal coding. With natural stimulation, activity in neighbouring neurons becomes decorrelated and more specialized (Vinje and Gallant 2000;Yen et al 2007). As stimulus complexity increases, therefore, a majority of neurons will receive net-inhibition, while a minority will receive net-excitation.…”

“…In this paper we focus on the spatial organization of contextual modulation under wide-field stimulation. This means that we will only briefly touch on a number of other relevant phenomena, including the increased sparseness of the neuronal code in the presence of visual context beyond the RF (Vinje and Gallant 2000;Yen et al 2007), the effect of visual working memory on the modulation of neural responses (Super et al 2001;Harrison and Tong 2009), and the influence of contextual stimuli on response latency profiles (Kapadia et al 1999;Li et al 2000;Huang and Paradiso 2005). In the section ''Mechanisms of horizontal integration into V1'', however, we will discuss in some detail the relevance of spatiotemporal dynamics of V1, as well as motion in the visual field induced by saccadic activity.…”