Temporal Properties of Inputs to Direction-Selective Neurons in Monkey V1

Abstract

. Motion in the visual scene is processed by direction-selective neurons in primary visual cortex. These cells receive inputs that differ in space and time. What are these inputs? A previous single-unit recording study in anesthetized monkey V1 proposed that the two major streams arising in the primate retina, the M and P pathways, differed in space and time as required to create direction selectivity. We confirmed that cortical cells driven by P inputs tend to have sustained responses. The M pathway, however, as assessed by recordings in layer 4C␣ and from cells with high contrast sensitivity, is not purely transient. The diversity of timing in the M stream suggests that combinations of M inputs, as well as of M and P inputs, create direction selectivity. I N T R O D U C T I O NDirection-selective (DS) neurons discriminate the direction of moving stimuli by obtaining inputs with receptive fields that differ in space and in time. For one direction of motion, the inputs fire at about the same time (in phase) because the spatial and temporal differences cancel each other. In the opposite direction, the input activity is not as synchronous (out of phase). That is, stimulus direction is translated into relative timing. A wide variety of mechanisms can convert these timing differences into divergent postsynaptic activities.Robust direction selectivity depends on approximately quarter-cycle phase differences ("spatiotemporal quadrature," in one direction the quarter cycles subtract to 0, and in the other they sum to a half-cycle). Ideally, a DS cell would obtain inputs that differ by a quarter cycle. Spatially, such inputs exist in the form of simple cells with overlapping receptive fields that differ purely in phase, such as even and odd symmetric fields with ON-OFF-ON and ON-OFF arrangements, respectively, for example. This has led some investigators to examine whether DS cells might receive inputs from non-DS cells that are in spatiotemporal quadrature. DeValois et al. (2000) showed that non-DS cells of these types exist in macaque V1. On the other hand, Peterson et al. (2004) argued that this scheme does not seem to work for cat V1.Actual, as opposed to ideal, DS cells do not receive inputs from just two non-DS cells that are in approximate spatiotemporal quadrature. Instead, multiple inputs converge on DS cells, including both inhibitory and excitatory cortical inputs as well as direct excitation from the LGN. The spatial relationships among these inputs could vary in position as well as in spatial phase. We understand how these positional differences among receptive fields originate in the spatial distribution of retinal cells. The more compelling question is, where do the different timings arise?In the cat, these timings originate in the retina, where a range of sustained and transient responses is generated. The distribution of timing is extended in the LGN, where additional temporal phase differences are created at low temporal frequencies (Saul and Humphrey 1990). Low temporal frequencies are of interest bec...

Development of Temporal Response Properties and Contrast Sensitivity of V1 and V2 Neurons in Macaque Monkeys

“…All V1 neurons, infants or adults, exhibited a "band-pass" profile. This result is different from the previous studies reporting that a substantial proportion of V1 neurons, particularly simple cells, exhibited "low-pass" tuning profiles (e.g., DeValois et al 2000;Saul et al 2005). However, we encountered more V2 neurons that exhibited "low-pass" tuning profiles at 2 (5%) and 4 wk (4%) than at 8 wk (1%) or in adults (0.6%).…”

A Dynamic Nonlinearity and Spatial Phase Specificity in Macaque V1 Neurons

“…In one case in layer 2/3 (PR, 1.2) and one in layer 4 (PR, 1.8), the rebound response was larger than the onset response at any phase; this is usually called a "lagged" response (cf. Saul et al, 2005). Excluding the one lagged cell in layer 2/3, the two largest PR values in layer 2/3 were 0.23 and 0.15; all of the remaining values were Ͻ0.1.…”

“…A completely monophasic response of this sort is almost never seen in response to reverse correlation stimuli in the LGN; even the most extreme neurons in cat and macaque LGN still have negative rebounds that are on the order of 20% of the area of the positive lobe (Alonso et al, 2001;Reid and Shapley, 2002). But monophasic impulse responses are observed in input layers in cat and macaque V1 (Alonso et al, 2001;Saul et al, 2005). Note that as with the step stimuli, the lack of an excitatory response from opposite-phase stimuli does not by itself indicate the presence of a nonlinearity.…”

Concurrent Encoding of Frequency and Amplitude Modulation in Human Auditory Cortex: MEG Evidence

“…In an ITD discrimination model study, Hancock and Delgutte (2004) have also proposed that the involvement of a phase shift mechanism in a system of solely internal delays could predict psychophysical performances more accurately. In the visual domain, "lagged cells" have been reported in both LGN and V1 (DeValois et al 2000;Saul and Humphrey 1990;Saul et al 2005). These cells show a specific lagged phase (e.g., by 90°) in their responses compared with ordinary "nonlagged cells" and are argued to solve the problem of encoding long and variable delays because a given phase difference provides longer time differences at low frequencies.…”