An architectural hypothesis for direction selectivity in the visual cortex: the role of spatially asymmetric intracortical inhibition

Abstract

Abstract. Within a linear ®eld approach, an architectural model for simple cell direction selectivity in the visual cortex is proposed. The origin of direction selectivity is related to recurrent intracortical interactions with a spatially asymmetric character along the axis of stimulus motion. No explicit asymmetric temporal mechanisms are introduced or adopted. The analytical investigation of network behavior, carried out under the assumption of a linear superposition of geniculate and intracortical contributions, shows that motion sensitivity of the resulting receptive ®elds emerges as a dynamic property of the cortical network without any feed-forward direction selectivity bias. A detailed analysis of the eects of the architectural characteristics of the cortical network on directionality and velocityresponse curves was conducted by systematically varying the model's parameters. IntroductionRecent theoretical and neurophysiological studies (DeAngelis et al. 1993a,b;Hamilton et al. 1989;McLean et al. 1994; Reid et al. 1991;Tolhurst and Dean 1991) pointed out that the origin of direction selectivity can be related to the linear space-time receptive ®eld structure of simple cells. A large class of simple cells shows a very speci®c space-time behavior in which the spatial phase of the receptive ®eld changes gradually as a function of time. This results in receptive ®eld pro®les that tilt along an oblique axis in the space-time domain (i.e., they are space-time inseparable). Accurate estimates of the velocity components to which the cell is selective (the preferred speed of motion) can be derived by measuring the slope of oriented receptive ®eld subregions in the space-time domain. Since lateral geniculate nucleus (LGN) cells do not exhibit tilted subregions, the origin of space-time inseparability must take place within the striate cortex. In general, the construction of inseparable simple-cell receptive ®elds implies a position-dependent alteration of the temporal response characteristics of the aerent inputs, presumably associated with cortical circuits characterized by asymmetric architectural schemes in space and/or time (for a review, see Koch and Hildreth 1987). Several models have been proposed. Some postulate the combination of spatially oset geniculate receptive ®elds with dierent temporal dynamics (Mastronarde 1987;Saul and Humphrey 1990;Wimbauer et al. 1994Wimbauer et al. , 1997. Others assume intracortical interactions among separable simple-cell receptive ®elds, possibly mediated by cortical interneurons (Ganz 1984;Ru et al. 1987;Sillito 1977;Somers et al. 1995). Most models, however, do not consider explicit recurrent asymmetric intracortical processes, and furthermore, a clear distinction between the roles of purely spatial and purely temporal mechanisms has not yet been made.In this paper, we point out that a purely spatial asymmetry is sucient to generate directional selectivity when spatially asymmetric contributions arise through recurrent intracortical inhibitory circuits. Therefore, the spac...

Motion detection, noise reduction, texture suppression, and contour enhancement by spatiotemporal Gabor filters with surround inhibition

“…The speed of the Gaussian envelope only affects the strength of the response for optimal versus nonoptimal stimulus direction and speed, but it has no influence on the preferred speed, which 123 is determined only by the phase speed of the moving cosine wave. The origin of direction and speed tuning properties, although not addressed in the current models, can be due to linear superposition of geniculate and intracortical contributions (Sabatini and Solari 1999). Further, these models have a functional link to the classical Reichardt model (Reichardt 1961) because of their relation to the energy model (Adelson and Bergen 1985).…”

Development of Response Timing and Direction Selectivity in Cat Visual Thalamus and Cortex

“…These models practically all posit intracortical mechanisms to generate temporal differences. Examples include NMDA receptor-mediated excitation (Maex and Orban, 1996), timing differences between excitatory and inhibitory synapses (Sabatini and Soleri, 1999), GABA B receptor-mediated inhibition (Suarez et al, 1995), temporal filtering induced by feedback (Suarez et al, 1995;Sabatini and Soleri, 1999), and depressing synapses (Chance et al, 1998). All of these mechanisms exist in the visual cortex and change timing, but none of these hypotheses for the origin of DS have been tested experimentally.…”

Spontaneously emerging direction selectivity maps in visual cortex through STDP

“…With the primary visual cortex being the first level at which these selectivities are found, it is evident that either thalamocortical and/or intracortical processing must be responsible for direction selectivity. In addition, the realization through feedforward or recurrent circuits, the role of inhibition, the spatiotemporal summation of channels of different temporal response characteristics, and contributions of short-and longterm plasticity have been considered in a multitude of experimental and theoretical investigations (Suarez et al 1995;Wimbauer et al 1997;Mineiro and Zipser 1998;Livingstone 1998;Sabatini and Solari 1999;Rao and Sejnowski 2001;Senn et al 2002;Roerig et al 2003;Shon et al 2004).…”