Second-order neuronal responses to contrast modulation stimuli in primate visual cortex

Abstract

Responses to contrast modulation (CM) and other second-order stimuli have been extensively studied in human psychophysics and neurophysiology in the cat. However the neuronal substrates of second-order responses in non-human primates remain poorly understood. To address this issue we have recorded single neurons in area V2 of anesthetized, paralyzed, carefully refracted macaque monkeys, using both CM stimuli as well as conventional luminance modulation (LM) gratings presented on a linearized CRT monitor. CM stimuli were constructed from stationary sinewave grating carriers, which were modulated by drifting envelope gratings of a lower spatial frequency. Initially using envelope parameters matched to each neuron's optimal LM grating, we systematically varied carrier spatial frequency at a series of carrier orientations. About one-third of visually responsive V2 neurons responded to CM stimuli with a pronounced selectivity to carrier spatial frequencies that were clearly outside the neuron’s passband for LM gratings, and therefore genuine second-order responses rather than luminance artifacts. Many of these neurons were also quite selective to carrier orientation; different neurons were selective for different carrier spatial frequencies and orientations. Using carrier parameters optimized for each neuron, we verified that tuning to CM envelope spatial frequency and orientation was very similar to that for LM gratings. Neurons were tuned to carrier spatial frequencies that were typically 2-4 octaves higher than their optimal envelope spatial frequencies. These results are distinct from CM responses arising from surround suppression (Tanaka & Ohzawa, J Neurophysiol, 2009; Hallum & Movshon, VSS, 2011), which show optimal carrier/envelope frequency ratios of about two. However they more resemble previous human psychophysics for CM (Sutter et al, Vis Res 1995; Dakin & Mareschal, Vis Res, 2000) and some other kinds of second-order stimuli (Kingdom & Keeble, Vis Res, 1999; Meso & Hess, Vis Res 2010), which are best detected at higher carrier/envelope frequency ratios.

Meeting abstract presented at VSS 2013