Alan B. Saul

Temporal-frequency tuning of direction selectivity in cat visual cortex.

Responses of 71 cells in areas 17 and 18 of the cat visual cortex were recorded extracellularly while stimulating with gratings drifting in each direction across the receptive field at a series of temporal frequencies. Direction selectivity was most prominent at temporal frequencies of 1-2 Hz. In about 20% of the total population, the response in the nonpreferred direction increased at temporal frequencies of around 4 Hz and direction selectivity was diminished or lost. In a few cells the preferred direction reversed. One consequence of this behavior was a tendency for the preferred direction to have lower optimal temporal frequencies than the nonpreferred direction. Across the population, the preferred direction was tuned almost an octave lower. In spite of this, temporal resolution was similar in the two directions. It appeared that responses in the nonpreferred direction were suppressed at low frequencies, then recovered at higher frequencies. This phenomenon might reflect the convergence in visual cortex of lagged and nonlagged inputs from the lateral geniculate nucleus. These afferents fire about a quarter-cycle apart (i.e. are in temporal quadrature) at low temporal frequencies, but their phase difference increases to a half-cycle by about 4 Hz. Such timing differences could underlie the prevalence of direction-selective cortical responses at 1 and 2 Hz and the loss of direction selectivity in many cells by 4 or 8 Hz.

Laminar differences in the spatiotemporal structure of simple cell receptive fields in cat area 17

Previous studies of cat visual cortex have shown that the spatiotemporal (S-T) structure of simple cell receptive fields correlates with direction selectivity. However, great heterogeneity exists in the relationship and this has implications for models. Here we report a laminar basis for some of the heterogeneity. S-T structure and direction selectivity were measured in 101 cells using stationary counterphasing and drifting gratings, respectively. Two procedures were used to assess S-T structure and its relation to direction selectivity. In the first, the S-T orientations of receptive fields were quantified by fitting response temporal phase versus stimulus spatial phase data. In the second procedure, conventional linear predictions of direction selectivity were computed from the amplitudes and phases of responses to stationary gratings. Extracellular recording locations were reconstructed histologically. Among direction-selective cells, S-T orientation was greatest in layer 4B and it correlated well (r = 0.76) with direction selectivity. In layer 6, S-T orientation was uniformly low, overlapping little with layer 4B, and it was not correlated with directional tuning. Layer 4A was intermediate in S-T orientation and its relation (r = 0.46) to direction selectivity. The same laminar patterns were observed using conventional linear predictions. The patterns do not reflect laminar differences in direction selectivity since the layers were equivalent in directional tuning. We also evaluated a model of linear spatiotemporal summation followed by a static nonlinear amplification (exponent model) to account for direction selectivity. The values of the exponents were estimated from differences between linearly predicted and actual amplitude modulations to counterphasing gratings. Comparing these exponents with another exponent--that required to obtain perfect matches between linearly predicted and measured directional tuning--indicates that an exponent model largely accounts for direction selectivity in most cells in layer 4, particularly layer 4B, but not in layer 6. Dynamic nonlinearities seem essential for cells in layer 6. We suggest that these laminar differences may partly reflect the differential involvement of geniculocortical and intracortical mechanisms.

Hebbian learning and the development of direction selectivity: The role of geniculate response timings

Zero-sum Hebbian learning rules that reinforce well correlated inputs have been used by others to model the competitive self-organization of afferents from the lateral geniculate nucleus to produce orientation selectivity and ocular dominance columns. However, the application of these simple Hebbian rules to the development of direction selectivity (DS) is problematic because the best correlated inputs are those that are well correlated in both the preferred and nonpreferred directions of motion. Such afferents would combine to produce non-DS cortical units. Afferents that are in spatiotemporal quadrature would combine to produce DS cortical units, but are poorly correlated in the nonpreferred direction. In this paper, the development of DS is reduced to the problem of associating a pair of units in spatiotemporal quadrature in the face of competition from a third, non-quadrature unit. As expected, simple Hebbian learning rules perform poorly at associating the quadrature pair. However, two additional Heb...

Adaptation aftereffects in single neurons of cat visual cortex: Response timing is retarded by adapting

Extracellular single-unit recordings were made from simple cells in area 17 of anesthetized cats. Cells were tested with drifting gratings under control and adapted conditions. Response amplitude and phase were measured as a function of either contrast or temporal frequency. Adapting not only reduces amplitude, but also retards phase. Adaptation alters the responses of simple cells in a particular way: the onset of the response to each cycle of a sinusoidally modulate stimulus is delayed. Once cells start to respond during each cycle, however, they generally recover to control levels, and the offset of the response is unaffected by adapting. The timing aftereffects are independent of the amplitude aftereffects. Timing aftereffects are tuned around the adapting temporal frequency, with a bias toward lower temporal frequencies. Adaptation thus modifies cortical responses even more specifically then previously thought. Firing rates are depressed primarily at response onset, even after several stimulus cycles have occurred following the end of adapting. Because all cells appear to adapt in this way, the data offer an opportunity to theorize about cortical connectivity. One implication is that inhibition onto a simple cell arises from other simple cells with similar response properties that fire a half-cycle out of phase with the target cell.

Visual cortical simple cells: who inhibits whom.

Simple cells display a specific adaptation aftereffect when tested with drifting gratings. The onset of the response to each cycle of the grating is delayed after adapting, but the offset is unaffected. Testing with stationary bars whose luminance was modulated in time revealed that aftereffects occur only at certain points in both space and time. The aftereffects seen with moving stimuli were predicted from those seen with stationary stimuli. These adaptation experiments suggest a model that consists of mutually inhibitory simple cells that are in spatiotemporal quadrature. The inhibition is appropriately localized in space and time to create the observed aftereffects. In this model, inhibition onto direction-selective simple cells arises from simple cells with the same preferred direction.

The Emergence of Direction Selectivity in Cat Primary Visual Cortex

Publisher Summary The emergence of direction selectivity in layer 4 of cat primary visual cortex depends on a number of mechanisms, both thalamocortical and intracortical. Lagged and nonlagged lateral geniculate nucleus (LGN) cells provide the cortex with a range of timings, or response phases, that serve as initial substrates for producing response timing gradients across receptive fields. This is particularly important at low temporal frequencies. These gradients induce directional tuning. Gradients might be established by direct convergence of afferents with spatially and temporally offset receptive fields, by indirect convergence via other simple cells with certain spatiotemporal relationships to their targets, or, most likely, by both mechanisms. Inhibitory interactions among simple cells appear to contribute to direction selectivity (DS) mainly by creating or enhancing spatiotemporal (S–T) inseparable receptive-field structure. Recurrent excitatory interactions enhance DS by amplifying suprathreshold responses. DS among most layer 4 simple cells can be explained by linear/nonlinear (LN) models in which quasilinear summation of synaptic potentials across an S–T inseparable receptive field induces directional tuning that is then enhanced by relatively simple nonlinear processes associated with spike generation.