We recorded from single neurons in the middle temporal visual area (MT) of the macaque monkey and studied their direction and orientation selectivity. We also recorded from single striate cortex (V1) neurons in order to make direct comparisons with our observations in area MT. All animals were immobilized and anesthetized with nitrous oxide. Direction selectivity of 110 MT neurons was studied with three types of moving stimuli: slits, single spots, and random-dot fields. All of the MT neurons were found to be directionally selective using one or more of these stimuli. MT neurons exhibited a broad range of direction-tuning bandwidths to all stimuli (minimum = 32 degrees, maximum = 186 degrees, mean = 95 degrees). On average, responses were strongly unidirectional and of similar magnitude for all three stimulus types. Orientation selectivity of 89 MT neurons was studied with stationary flashed slits. Eighty-three percent were found to be orientation selective. Overall, orientation-tuning bandwidths were significantly narrower (mean = 64 degrees) than direction-tuning bandwidths for moving stimuli. Moreover, responses to stationary-oriented stimuli were generally smaller than those to moving stimuli. Direction selectivity of 55 V1 neurons was studied with moving slits; orientation selectivity of 52 V1 neurons was studied with stationary flashed slits. In V1, compared with MT, direction-tuning bandwidths were narrower (mean = 68 degrees). Moreover, V1 responses to moving stimuli were weaker, and bidirectional tuning was more common. The mean orientation-tuning bandwidth in V1 was also significantly narrower than that in MT (mean = 52 degrees), but the responses to stationary-oriented stimuli were of similar magnitude in the two areas. We examined the relationship between optimal direction and optimal orientation for MT neurons and found that 61% had an orientation preference nearly perpendicular to the preferred direction of motion, as is the case for all V1 neurons. However, another 29% of MT neurons had an orientation preference roughly parallel to the preferred direction. These observations, when considered together with recent reports claiming sensitivity of some MT neurons to moving visual patterns (39), suggest specific neural mechanisms underlying pattern-motion sensitivity in area MT. These results support the notion that area MT represents a further specialization over area V1 for stimulus motion processing. Furthermore, the marked similarities between direction and orientation tuning in area MT in macaque and owl monkey support the suggestion that these areas are homologues.
The contrast sensitivity function (CSF) predicts functional vision better than acuity, but long testing times prevent its psychophysical assessment in clinical and practical applications. This study presents the quick CSF (qCSF) method, a Bayesian adaptive procedure that applies a strategy developed to estimate multiple parameters of the psychometric function (A. B. Cobo-Lewis, 1996; L. L. Kontsevich & C. W. Tyler, 1999). Before each trial, a one-step-ahead search finds the grating stimulus (defined by frequency and contrast) that maximizes the expected information gain (J. V. Kujala & T. J. Lukka, 2006; L. A. Lesmes et al., 2006), about four CSF parameters. By directly estimating CSF parameters, data collected at one spatial frequency improves sensitivity estimates across all frequencies. A psychophysical study validated that CSFs obtained with 100 qCSF trials (~10 min) exhibited good precision across spatial frequencies (SD < 2–3 dB) and excellent agreement with CSFs obtained independently (mean RMSE = 0.86 dB). To estimate the broad sensitivity metric provided by the area under the log CSF (AULCSF), only 25 trials were needed to achieve a coefficient of variation of 15–20%. The current study demonstrates the method’s value for basic and clinical investigations. Further studies, applying the qCSF to measure wider ranges of normal and abnormal vision, will determine how its efficiency translates to clinical assessment.
We recorded from single neurons in visual area MT of the macaque in order to examine the spatial distribution of its directionally selective cells. The animals were paralyzed and anesthetized with nitrous oxide. All MT neurons (n = 614) responded better to moving stimuli than to stationary stimuli. For 55% of the neurons, responses to moving stimuli were independent of stimulus color, shape, length, or orientation. For the remaining cells, stimulus length affected the response magnitude and tuning bandwidth but not the preferred direction. MT neurons were divided into four categories on the basis of their sensitivity to moving stimuli: 60% responded exclusively to one direction of motion, 24% responded best to one direction with a weaker response in the opposite direction, 8% responded equally well to two opposite directions of motion, and 8% responded equally well to all directions of motion. The direction preferences of successively sampled cells on a penetration either changed by small increments or occasionally by approximately 180 degrees. Thus, there is a systematic representation of direction of motion. The representation of axis of motion, i.e., the orientation of the path along which a stimulus moves, is more continuous than the representation of direction of motion. There was a systematic relationship between penetration angle and rate of change of preferred axis of motion, indicating that cells with a similar axis of motion preference are arranged in vertical columns. Furthermore, axis of motion columns appear to exist in the form of continuous slabs in area MT. The size of these slabs is such that 180 degrees of axis of motion are represented in 400-500 micron of cortex. There was also a systematic relationship between penetration angle and frequency of 180 degrees reversals, indicating that cells with a similar direction of motion preference are also organized in vertical columns and cells with opposite direction preferences are located in adjacent columns within a single axis of motion column. Just as in macaque striate cortex where approximately 500 micron of cortex contain the mechanism for the local analysis of stimulus orientation, so in MT approximately 500 micron of cortex contain the mechanism for the local analysis of stimulus motion.
Although motion-sensitive neurons in macaque middle temporal (MT) area are conventionally characterized using stimuli whose velocity remains constant for 1-3 s, many ecologically relevant stimuli change on a shorter time scale (30-300 ms). We compared neuronal responses to conventional (constant-velocity) and time-varying stimuli in alert primates. The responses to both stimulus ensembles were well described as rate-modulated Poisson processes but with very high precision (approximately 3 ms) modulation functions underlying the time-varying responses. Information-theoretic analysis revealed that the responses encoded only approximately 1 bit/s about constant-velocity stimuli but up to 29 bits/s about the time-varying stimuli. Analysis of local field potentials revealed that part of the residual response variability arose from "noise" sources extrinsic to the neuron. Our results demonstrate that extrastriate neurons in alert primates can encode the fine temporal structure of visual stimuli.
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