Switching between off and on in the macaque visual system

Wyeth Bair, James R. Cavanaugh, Matthew A. Smith and J. Anthony Movshon

New York University

At multiple stages in the visual system, neurons can be driven rapidly from near minimum to near maximum firing rate (turned on) or from near maximum to near minimum rate (turned off). We measured the timing of single neuron responses to on-to-off and off-to-on transitions in the LGN, V1, and area MT/V5 of the anesthetized macaque monkey in order to understand how signals which support the on and off states interact at the transition boundaries and how the interactions differ across visual areas and classes of neurons.

Our stimuli were random binary sequences in which either a preferred stimulus (P, which drove the cell maximally) or an anti-preferred stimulus (A, giving minimal response) was shown on each video frame at 100Hz. We also used ternary random sequences which included a neutral stimulus (N). Typically, P was an optimized sine grating, A was counterphase (LGN and V1) or orthogonal to P (V1), and N was mean gray. For direction selective (DS) cells, P moved in the preferred direction, A moved in the opposite direction, and N was static. We tested the center and surround in LGN, the classical receptive field and surround in V1, and DS cells in V1 and MT/V5.

Almost always, the response latency for on-to-off (P-->A) transitions was shorter than that for off-to-on (A-->P) transitions. In particular, the decrease in firing rate for P-->A transitions began sooner than the rate increase for A-->P transitions, and the delay for the A-->P response was often less when A was present longer. With ternary stimuli, the N-->P and N-->A responses showed little or no timing difference for the LGN and for DS cells in V1 and MT/V5. However, for orientation selectivity in V1, the timing asymmetry persisted for N-->P and N-->A responses. Our results are consistent with the notion that anti-preferred stimuli place neurons in a hyperpolarized state, delaying the response when a preferred stimulus is applied. The delay depends on both the duration of A and on the strength of P. An integrate-and-fire model can reproduce the observed latency asymmetry; however, variations in the typical behavior across classes of neurons reveal differences in mechanisms that process different visual features.