Hao Sun

Suppressive Surrounds and Contrast Gain in Magnocellular-Pathway Retinal Ganglion Cells of Macaque

The modulation sensitivity of visual neurons can be influenced by remote stimuli which, when presented alone, cause no change in the ongoing discharge rate of the neuron. We show here that the extraclassical surrounds that underlie these effects are present in magnocellular-pathway (MC) but not in parvocellular-pathway (PC) retinal ganglion cells of the macaque. The response of MC cells to drifting gratings and flashing spots was halved by drifting or contrast-reversing gratings surrounding their receptive fields, but PC cell responses were unaffected. The suppression cannot have arisen from the classical receptive field, or been caused by scattered light, because it could be evoked by annuli that themselves caused little or no response from the cell, and is consistent with the action of a divisive suppressive mechanism. Suppression in MC cells was broadly tuned for spatial and temporal frequency and greater at high contrast. If perceptual phenomena with similar stimulus contexts, such as the “shift effect” and saccadic suppression, have a retinal component, then they reflect the activity of the MC pathway.

The temporal properties of the response of macaque ganglion cells and central mechanisms of flicker detection

This analysis assesses sensitivity of primate ganglion cells to sinusoidal modulation as a function of temporal frequency, based on the structure of their impulse trains; sensitivity to luminance and chromatic modulation was compared to human psychophysical sensitivity to similar stimuli. Each stimulus cycle was Fourier analyzed, and response amplitudes subjected to neurometric analysis; this assumes a detector with duration inversely proportional to frequency, that is, the stimulus epoch analyzed is a single cycle rather than a fixed duration, and provides an upper bound for a detection by an observer who bases judgments on a single cell. Signal-to-noise ratio for a given Fourier amplitude rapidly decreased with temporal frequency. This is a consequence of the statistics of impulse trains making up the response; at higher temporal frequencies, there are fewer impulses per cycle. Performance of this single-cell observer was then compared with that of modeled central detection mechanisms of fixed duration. For chromatic modulation, a filter/detector with a time constant of approximately 40 ms operating upon the parvocellular (PC) pathway provided a match to psychophysical results, whereas for luminance modulation, a filter/detection mechanism operating upon the magnocellular (MC) pathway with a time constant of approximately 5-10 ms provided a suitable match. The effects of summation and nonlinear interactions between cell inputs to detection are also considered in terms of enhanced sensitivity and sharpness of thresholds, that is, the steepness of the neurometric function. For both luminance (MC cells) and chromatic modulation (PC cells), restricted convergence (<20 cells) appears adequate to provide sharp thresholds and sensitivity comparable to psychophysical performance.

The spatiotemporal precision of ganglion cell signals: a comparison of physiological and psychophysical performance with moving gratings

Comparison of the spatiotemporal information delivered by ganglion cells with human psychophysical performance may give insight to how retinal information is utilized by cortical mechanisms, and constrain models of spatiotemporal processing. Ganglion cells responses were measured with drifting gratings of various spatial and temporal frequencies and contrasts. The spatiotemporal precision of cell responses was estimated in terms of a noise measure and phase variation, and compared to human vernier performance. Noise and phase variation of magnocellular (MC) cells was least at low temporal frequencies, despite their transient responses. The patterns of spatiotemporal precision of MC cells resembled the patterns of human vernier thresholds while those of parvocellular cells did not, implying use of MC cells signals in these tasks. The analysis further implied that cortical mechanisms must perform a sophisticated spatiotemporal analysis over local ganglion cell arrays.

Transient cells can be neurometrically sustained: the positional accuracy of retinal signals to moving targets

The spatial accuracy inherent in retinal ganglion cell responses to moving targets was investigated by measuring trial-to-trial variability in response locus. When moving bars were used as stimuli, analysis of impulse trains showed that parafoveal cells of the magnocellular (MC) pathway provided a consistently accurate spatial signal over a range of target velocities up to ~8 deg/sec. Parvocellular (PC) pathway cells delivered less accurate signals even at low velocities, and their signals became even less accurate at higher target speeds. Human vernier performance in parafovea resembled the physiological MC-cell result, which suggests this feature of MC-cell behavior is functionally utilized. A similar result held with moving gratings; the highest signal-to-noise ratio for MC-cells occurred at low temporal frequencies. Psychophysical vernier thresholds to grating targets resembled phase variability of MC-cell responses as a function of temporal frequency. The analyses of physiological data utilized both the number of impulses a cell generates and their timing; MC-cells responses may have low peak rates to slow moving stimuli compared to fast stimuli, but a spatially precise signal may be derived because many impulses are evoked at lower speeds. The results show that transient neurons can yield precise information about slowly moving stimuli, provided appropriate central mechanisms for extracting this information are present. Such central mechanisms would require either a long integration time or a suitable spatiotemporal filter that integrates over the ganglion array. Because accurate vernier performance can be achieved with brief presentations, the latter alternative is indicated.

Macaque ganglion cells, light adaptation, and the Westheimer paradigm

Retinal adaptation mechanisms are considered relative to the Westheimer paradigm. Responses to a probe presented upon pedestals were obtained from macaque ganglion cells. On-center magnocellular (MC) cell responses decreased to a plateau as pedestal diameter increased, consistent with operation of a local adaptation pool. Off-center cells also demonstrated a vigorous response with small pedestals, but as pedestal size increased, responsivity decreased and then partially recovered as pedestals encroached upon the surround. The response trough was due to a profound suppression of maintained activity. Comparison with psychophysical data suggests a multiple physiological substrate for the Westheimer paradigm, involving an interaction between adaptation pools, changes in maintained firing due to center-surround mechanisms and a cortical component.

Comparison of ganglion cell signals and psychophysical localization of moving targets can help define central motion mechanisms

Vernier acuity thresholds can be related to visibility of targets. This is considered in relation to retinal signals. Spatial precision of macaque ganglion cell responses to moving targets was assessed by neurometric analysis and compared with psychophysical performance. Under some conditions the amplitude of ganglion cell signals per se may relate target visibility to spatial precision of psychophysical performance. Other conditions are more complex; we suggest central mechanisms may adapt their properties, eg their dimensions, depending on the stochastic properties of ganglion cell signals. Thus, the relation of Vernier acuity to the visibility of targets is a rule of thumb which has a complex relation to physiological substrates.