Macaque V1 responses to 2nd-order contrast-modulated stimuli and the possible subcortical and cortical contributions.

Natural images comprise contours and boundaries defined by 1st-order luminance-modulated (LM) cues that are readily encoded by V1 neurons, and 2nd-order contrast-modulated (CM) cues that carry local, but not over-the-space, luminance changes. The neurophysiological foundations for CM processing remain unsolved. Here we used two-photon calcium imaging to demonstrate that V1 superficial-layer neurons respond to both LM and CM gratings in awake, fixating, macaques, with overall LM responses stronger than CM responses. Furthermore, adaptation experiments revealed that LM responses were similarly suppressed by LM and CM adaptation, with moderately larger effects by iso-orientation adaptation than by orthogonal adaptation, suggesting that LM and CM orientation responses likely share a strong orientation-non-selective subcortical origin. In contrast, CM responses were substantially more suppressed by iso-orientation than by orthogonal LM and CM adaptation, likely suggesting stronger orientation-specific intracortical influences for CM responses than for LM responses, besides shared orientation-non-selective subcortical influences. These results thus may indicate a subcortical-to-V1 filter-rectify-filter mechanism for CM processing: Local luminance changes in CM stimuli are initially encoded by orientation-non-selective subcortical neurons, and the outputs are half-wave rectified, and then summed by V1 neurons to signal CM orientation, which may be further substantially refined by intracortical influences.

A supramodal and conceptual representation of subsecond time revealed with perceptual learning of temporal interval discrimination.

Subsecond time perception has been frequently attributed to modality-specific timing mechanisms that would predict no cross-modal transfer of temporal perceptual learning. In fact, perceptual learning of temporal interval discrimination (TID) reportedly shows either no cross-modal transfer, or asymmetric transfer from audition to vision, but not vice versa. However, here we demonstrate complete cross-modal transfer of auditory and visual TID learning using a double training paradigm. Specifically, visual TID learning transfers to and optimizes auditory TID when the participants also receive exposure to the auditory temporal interval by practicing a functionally orthogonal near-threshold tone frequency discrimination task at the same trained interval. Auditory TID learning also transfers to and optimizes visual TID with additional practice of an orthogonal near-threshold visual contrast discrimination task at the same trained interval. Practicing these functionally orthogonal tasks per se has no impact on TID thresholds. We interpret the transfer results as indications of a supramodal representation of subsecond time. Moreover, because TID learning shows complete transfer between modalities with vastly different temporal precisions, the sub-second time presentation must be conceptual. Double training may refine this supramodal and conceptual subsecond time representation and connect it to a new sense to improve time perception.

Functional organization of spatial frequency tuning in macaque V1 revealed with two-photon calcium imaging.

V1 neurons are functionally organized in orientation columns in primates. Whether spatial frequency (SF) columns also exist is less clear because mixed results have been reported. A definitive solution would be SF functional maps at single-neuron resolution. Here we used two-photon calcium imaging to construct first cellular SF maps in V1 superficial layers of five awake fixating macaques, and studied SF functional organization properties and neuronal tuning characteristics. The SF maps (850 × 850 µm2) showed weak horizontal SF clustering (median clustering index = 1.43 vs. unity baseline), about one sixth as strong as orientation clustering in the same sets of neurons, which argues against a meaningful orthogonal relationship between orientation and SF functional maps. These maps also displayed nearly absent vertical SF clustering between two cortical depths (150 & 300 µm), indicating a lack of SF columnar structures within the superficial layers. The underlying causes might be that most neurons were tuned to a narrow two-octave range of medium frequencies, and many neurons with different SF preferences were often spatially mixed, which disallowed finer grouping of SF tuning. In addition, individual SF tuning functions were often asymmetric, having wider lower frequency branches, which may help encode low SF information for later decoding.

Orientation Tuning and End-stopping in Macaque V1 Studied with Two-photon Calcium Imaging.

Orientation tuning is a fundamental response property of V1 neurons and has been extensively studied with single-/multiunit recording and intrinsic signal optical imaging. Long-term 2-photon calcium imaging allows simultaneous recording of hundreds of neurons at single neuron resolution over an extended time in awake macaques, which may help elucidate V1 orientation tuning properties in greater detail. We used this new technology to study the microstructures of orientation functional maps, as well as population tuning properties, in V1 superficial layers of 5 awake macaques. Cellular orientation maps displayed horizontal and vertical clustering of neurons according to orientation preferences, but not tuning bandwidths, as well as less frequent pinwheels than previous estimates. The orientation tuning bandwidths were narrower than previous layer-specific single-unit estimates, suggesting more precise orientation selectivity. Moreover, neurons tuned to cardinal and oblique orientations did not differ in quantities and bandwidths, likely indicating minimal V1 representation of the oblique effect. Our experimental design also permitted rough estimates of length tuning. The results revealed significantly more end-stopped cells at a more superficial 150 µm depth (vs. 300 µm), but unchanged orientation tuning bandwidth with different length tuning. These results will help construct more precise models of V1 orientation processing.

Plaid Detectors in Macaque V1 Revealed by Two-Photon Calcium Imaging.

Neuronal responses to one-dimensional orientations are combined to represent two-dimensional composite patterns; this plays a key role in intermediate-level vision such as texture segmentation. However, where and how the visual cortex starts to represent composite patterns, such as a plaid consisting of two superimposing gratings of different orientations, remains neurophysiologically elusive. Psychophysical and modeling evidence has suggested the existence of early neural mechanisms specialized in plaid detection [1-6], but the responses of V1 neurons to an optimally orientated grating are actually suppressed by a superimposing grating of different orientation (i.e., cross-orientation inhibition) [7, 8]. Would some other V1 neurons be plaid detectors? Here, we used two-photon calcium imaging [9] to compare the responses of V1 superficial-layer neurons to gratings and plaids in awake macaques. We found that many non-orientation-tuned neurons responded weakly to gratings but strongly to plaids, often with plaid orientation selectivity and cross-angle selectivity. In comparison, most (∼94%) orientation-tuned neurons showed more or less cross-orientation inhibition, regardless of the relative stimulus contrasts. Only a small portion (∼8%) of them showed plaid facilitation at off-peak orientations. These results suggest separate subpopulations of plaid and grating responding neurons. Because most of these plaid neurons (∼95%) were insensitive to motion direction, they were plaid pattern detectors, not plaid motion detectors.