Allen L. Humphrey

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.

Lagged Y cells in the cat lateral geniculate nucleus.

We report on the existence of lagged Y (YL) cells in the A laminae of the cat lateral geniculate nucleus (LGN) and on criteria for identifying them using visual and electrical stimulation. Like the lagged X (XL) cells described previously (Mastronarde, 1987a; Humphrey & Weller, 1988a), YL cells responded to a spot stimulus with an initial dip in firing and a delayed latency to discharge after spot onset, and an anomalously prolonged firing after spot offset. However, the cells received excitatory input from retinal Y rather than X afferents, and showed nonlinear spatial summation and other Y-like receptive-field properties. Three YL cells tested for antidromic activation from visual cortex were found to be relay cells, with long conduction latencies similar to those of XL cells. Simultaneous recordings of a YL cell and its retinal Y afferents show striking parallels between lagged X and Y cells in retinogeniculate functional connectivity, and suggest that the YL-cell response profile reflects inhibitory processes occurring within the LGN. The YL cells comprised approximately 5% of Y cells and approximately 1% of all cells in the A laminae. Although infrequently encountered in the LGN, they may be roughly as numerous as Y cells in the retina, and hence could fulfill an important role in vision.

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...

Cell types and response timings in the medial interlaminar nucleus and C-layers of the cat lateral geniculate nucleus

Previous evidence concerning the physiological cell classes in the medial interlaminar nucleus (MIN) has been conflicting. We reexamined the MIN using standard functional tests to distinguish X-, Y- and W-cells. Discharge patterns to flashing spots also were used to identify some cells as lagged or nonlagged, as previously done for the geniculate A-layers. Also, each cells response timing (latency and absolute phase) was measured from discharges to a spot undergoing sinusoidal luminance modulation. Of 71 MIN cells, 48% were Y, 27% were W, 8% were X, and 17% were unclassifiable. Lagged and nonlagged discharge profiles were observed in each cell group, with 28% of all cells being lagged. Lagged cells displayed a response suppression and long latency to discharge following spot onset, and a slow decay in firing at spot offset that was often preceded by a transient discharge. These profiles were indistinguishable from those of lagged cells in the A-layers. MIN cells also were heterogeneous in response timing, displaying a range of latency and absolute phase values similar to that in the A-layers. We extended these analyses to 27 cells in the geniculate C-layers. In layer C, 35% of cells were Y, 10% were X, 25% were W, and 30% were unclassifiable. About 11% had lagged profiles, and were X-cells or unclassifiable cells. Layers C1 and C2 contained only W-cells and no lagged profiles. The range of timings in the C-layers was somewhat narrower than in the MIN. Overall, these results show that the MIN contains a greater variety of functional cell classes than heretofore appreciated. Further, it appears that mechanisms which create different timing delays in the A-layers also exist in the MIN and layer C. These timings may contribute to direction selectivity in extrastriate cortex.

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.