Direction Selectivity of Synaptic Potentials in Simple Cells of the Cat Visual Cortex

Abstract

Direction selectivity of synaptic potentials in simple cells of the cat visual cortex. J. Neurophysiol. 78: 2772-2789, 1997. The direction selectivity of simple cells in the visual cortex is generated at least in part by nonlinear mechanisms. If a neuron were spatially linear, its responses to moving stimuli could be predicted accurately from linear combinations of its responses to stationary stimuli presented at different positions within the receptive field. In extracellular recordings, this has not been found to be the case. Although the extracellular experiments demonstrate the presence of a nonlinearity, the cellular process underlying the nonlinearity, whether an early synaptic mechanism such as a shunting inhibition or simply the spike threshold at the output, is not known. To differentiate between these possibilities, we have recorded intracellularly from simple cells of the intact cat with the whole cell patch technique. A linear model of direction selectivity was used to analyze the synaptic potentials evoked by stationary sine-wave gratings. The model predicted the responses of cells to moving gratings with considerable accuracy. The degree of direction selectivity and the time course of the responses to moving gratings were both well matched by the model. The direction selectivity of the synaptic potentials was considerably smaller than that of the intracellularly recorded action potential, indicating that a nonlinear mechanism such as threshold enhances the direction selectivity of the cell's output over that of its synaptic inputs. At the input stage, however, the cells apparently sum their synaptic inputs in a highly linear fashion. A more constrained test of linearity of synaptic summation based on principal component analysis was applied to the responses of direction-selective cells to stationary gratings. The analysis confirms that the summation in these cells is highly linear. The principal component analysis is consistent with a model in which direction selectivity in cortical simple cells is generated by only two subunits, each with a different receptive-field position and response time course. The response time course for each of the two subunits is derived for four analyzed cells. Each derived subunit is linear in spatial summation, suggesting that the neurons that comprise each subunit are either geniculate X-cells or receive their primary synaptic input from X-cells. The amplitude of the response of each subunit is linearly related to the contrast of the stimulus. The subunits are nonlinear in the time domain, however: the response to a stationary stimulus whose contrast is modulated sinusoidally in time is nonsinusoidal. The principal component analysis does not exclude models of direction selectivity based on more than two subunits, but such higher-order models would have to include the constraint that the extra subunits form a smooth continuum of interpolation between the properties derived from the two subunit solution.

Intrinsic and Extrinsic Contributions to Auditory Selectivity in a Song Nucleus Critical for Vocal Plasticity

“…The suprathreshold responsiveness (R FiringRate ) of cells with spiking activity was calculated by R FiringRate ϭ S FR Ϫ B FR , where S FR and B FR are the firing rates during each stimulus presentation and during a 1.0 -1.5 sec baseline period before each stimulus presentation, respectively. To assess subthreshold responsiveness in spiking cells, raw traces were first median-filtered (each point replaced by the median value of the surrounding 50 points, equivalent to 5 msec at our sample rate of 10 kHz); this removes very high-frequency events such as action potentials (which are ϳ1 msec in duration) and thus reduces action potential contamination of subthreshold changes in membrane potential [for an example, see Jagadeesh et al (1997), their Fig. 1].…”

“…In LMAN, greater suprathreshold than subthreshold selectivity could be evidence of local refinement at a single-cell level, for example, by a nonlinear thresholding mechanism (Jagadeesh et al, 1997). To compare subthreshold and suprathreshold song selectivity in single LMAN neurons, the subthreshold and suprathreshold responses of all cells (n ϭ 299) were normalized using z-scores (Fig.…”

Differences in the Time Course of Short-Term Depression Across Receptive Fields Are Correlated With Directional Selectivity in Electrosensory Neurons

“…It is therefore not surprising that the mechanisms that mediate directional selectivity to movement are quite diverse and vary across sensory modalities and species. In fact, these can take the form of different low-pass filters, as observed in the insect visual system (Borst 2007;Borst and Egelhaaf 1989), different dendritic integration in rabbit retinal ganglion cells (Taylor et al 2000;Yang and Masland 1992), and differential delays in mammalian visual cortex (Jagadeesh et al 1993(Jagadeesh et al , 1997. These mechanisms could be used in other spatiotemporal computations.…”

Representation of Sounds in Auditory Cortex of Awake Rats (Dissertation)

“…Recently, several laboratories introduced whole-cell recording techniques in-vivo in various sensory systems: auditory (DeWeese and Zador, 2006;Tan et al, 2004;Zador, 2003, 2005;Zhang et al, 2003), visual (Anderson et al, 2000;Carandini and Ferster, 2000;Ferster and Jagadeesh, 1992;Jagadeesh et al, 1993Jagadeesh et al, , 1997Pei et al, 1991), somatosensory (Brecht et al, 2003;Brecht and Sakmann, 2002;Bruno and Sakmann, 2006;Bureau et al, 2004;Petersen et al, 2003b;Zhu and Connors, 1999), and olfactory (Margrie and Schaefer, 2003;Schaefer et al, 2006).…”

“…2.5). We used 4 ms median filter, where each point in the voltage trace was replaced with a median of itself and 16 or 40 (depending on sampling rate) surrounding points (Jagadeesh et al, 1997). Therefore, large fast fluctuations (action potentials) were removed, while slower fluctuations (up to very fine details) were preserved.…”