Scale-invariance of receptive field properties in primary visual cortex

<p>Abstract</p> <p>Background</p> <p>Our visual system enables us to recognize visual objects across a wide range of spatial scales. The neural mechanisms underlying these abilities are still poorly understood. Size- or scale-independent representation of visual objects might be supported by processing in primary visual cortex (V1). Neurons in V1 are selective for spatial frequency and thus represent visual information in specific spatial wavebands. We tested whether different receptive field properties of neurons in V1 scale with preferred spatial wavelength. Specifically, we investigated the size of the area that enhances responses, i.e., the grating summation field, the size of the inhibitory surround, and the distance dependence of signal coupling, i.e., the linking field.</p> <p>Results</p> <p>We found that the sizes of both grating summation field and inhibitory surround increase with preferred spatial wavelength. For the summation field this increase, however, is not strictly linear. No evidence was found that size of the linking field depends on preferred spatial wavelength.</p> <p>Conclusion</p> <p>Our data show that some receptive field properties are related to preferred spatial wavelength. This speaks in favor of the hypothesis that processing in V1 supports scale-invariant aspects of visual performance. However, not all properties of receptive fields in V1 scale with preferred spatial wavelength. Spatial-wavelength independence of the linking field implies a constant spatial range of signal coupling between neurons with different preferred spatial wavelengths. This might be important for encoding extended broad-band visual features such as edges.</p

Spatio-temporal representations during eye movements and their neuronal correlates

During fast ballistic eye movements, so-called saccades, our visual perception undergoes a range of distinct changes. Sensitivity to luminance contrasts is reduced (saccadic suppression) and the localization of stimuli can be shifted in the direction of a saccade or is compressed around the saccade target. The temporal order of two stimuli can be perceived as inverted and the duration in between can be underestimated. The duration of a target change close to the saccade target can be overestimated, when the change occurs during the saccade (chronostasis). In my thesis I investigated the spatial and temporal profiles of peri-saccadic changes in human visual perception and explored how these might result from changes in neural activity of the macaque middle temporal area (MT). I found that peri-saccadic contrast sensitivity was only reduced by a constant factor across space when the data was analyzed in retinal coordinates (as opposed to screen coordinates), indicating that saccadic suppression occurs in an eye-centered frame of reference. I demonstrated that the found variations of saccadic suppression with the location of the stimulus appear to cause variations in the spatio-temporal pattern of another peri-saccadic misperception: chronostasis. I was able to show that, unlike previously assumed, the saccadic overestimation of time is not a spatially localized disturbance of time perception but instead spans across the whole visual field. I further determined that chronostasis is not dependent on the eye movement itself, but is rather a consequence of the visual stimulation induced by it. This result clearly segregates chronostasis from other peri-saccadic perceptual changes like saccadic suppression and the compression of space. To relate these findings to a potential neuronal basis of saccadic suppression and time perception, I measured neuronal responses of single cells in MT of an awake behaving macaque. The results provide relevant insight into the processing of stationary stimuli and pairs of stimuli during fixation and saccades in MT. Responses to the second of a pair of stimuli were strongly suppressed and response latencies increased even at onset asynchronies of about 100ms. The increase in latency is an important difference to the temporal dynamics previously reported in other brain areas as the frontal eye field in the frontal cortex and the superior colliculus in the midbrain. During saccades, response latencies to single high luminance stimuli remained unchanged. For stimuli shown during the second half of the saccade, the average responses were reduced. By comparison with responses to single stimuli at different luminance levels during fixation, I was able to show that the peri-saccadic response reduction found in MT quantitatively fit to what could be expected from known psychophysical measurements of peri-saccadic contrast sensitivity. Responses that were already reduced due to a preceding stimulus were however not subject to further reductions, indicating a possible interaction of these two response modulations. Saccadic suppression occurs in an eye-centered frame of reference with changes in perception compatible to changes in single cell activity in the macaque monkey MT. The peri-saccadic overestimation of time is influenced by saccadic suppression and the saccade-induced visual changes, but is not dependent on eye-movement related signals

Signal transformation and noise correlation in the primate dorsal stream during sensory decision-making

Neuroscientists have long sought a link between the activity of single neurons and our thoughts, perceptions and ultimately our mental experiences. As our senses provide the input into the brain, understanding the computations that transform signals along the sensory pathways has remained central to this endeavor. Remarkable progress has been made by studying neural correlates of perceptual decisions in motion-processing and oculomotor areas of the primate brain. In particular, when monkeys indicate their decisions about the direction of motion with eye movements, neurons in the middle temporal area (MT) represent the instantaneous motion evidence and neurons in the lateral intraparietal area (LIP) resemble the integration of motion evidence, effectively transforming the sensory signal into a decision variable. In the main body of this thesis, I describe the results of an effort to measure the sensorimotor transformation between MT and LIP on single trials. First, I describe a motion-discrimination task that is amenable to reverse correlation analysis, allowing the experimenter to measure the temporal dependencies of neural responses and choices on the instantaneous motion energy. I then use a unified statistical framework to analyze simultaneous recordings from both areas during decision-making. Primarily, I found that MT neurons exhibited time-varying sensitivity to motion direction, with important consequences for the behavior and neurophysiology in downstream areas. Individual LIP neurons also carried a signature of an integrated motion signal in their spike rates, however, it was unlikely that this signal results from direct MT input. Finally, I show that a biologically plausible simple decoder can perform as well as the monkey at coarse direction-discrimination task. In the appendix, I describe the results of pharmacological inactivations of MT and LIP and statistical models of single trial dynamics in LIP that were performed in collaboration with fellow graduate students, Leor Katz and Kenneth Latimer, respectively.Neuroscienc

Spike timing precision in the visual front-end

This thesis describes a series of investigations into the reliability of neural responses in the primary visual pathway. The results described in subsequent chapters are primarily based on extracellular recordings from single neurons in anaesthetized cats and area MT of an awake monkey, and computational model analysis. Comparison of spike timing precision in recorded and Poisson-simulated spike trains shows that spike timing in the front-end visual system is considerably more precise than one would expect on the basis of the time varying spike rate. Based on the nature of the measure that was used to quantify spike timing precision, this implies that spike trains in the visual front-end allow for an interesting decoding scheme. This encompasses optimal correlation detection, where temporal correlations are detected independent of straightforward synchronicity. This is described in chapters 1 and 2. Chapter 3 introduces a novel method: Motion Reverse Correlation (MRC), that was developed for measuring receptive field properties of motion selective cells in the visual cortex. Application of the method is illustrated with results obtained from area 18 and PMLS of anaesthetized cats and area MT in a fixating macaque monkey. In chapter 4, a conventional luminance white noise reverse correlation method is used to obtain spatio-temporal impulse responses of retinal ganglion cells, cells in the LGN and in area 17. These were then used to predict the responses of these cells to movie clips of natural scenes. Results show that conventional linear-static nonlinear models do not suffice to predict the recorded responses and suggest that dynamic nonlinear mechanisms should be taken into account also. As the quality of the predictions decreases from retina through area 17, it is concluded that these mechanisms become increasingly important at subsequent stages of information processing in the primary visual pathway. Chapter 5 focuses on the functional consequences of spike timing variability for visual motion detection. A bilocal correlator model is used to assess the time scale at which information is represented in the output of the retina and LGN, and its stimulus dependence. The pattern of results that we find is subsequently compared to the temporal limits for motion discrimination in a human psychophysics experiment. We find a close agreement between the results obtained in the two experiments and show that spike timing precision allows for correlation detection at very short time scales

The perception of second-order motion

In this thesis the notion of an independent non-linear channel for the perception of second- order motion is investigated. An examination of speed discrimination thresholds for first- and second-order bars and edges showed no differences in the patterns of response over changes in the temporal and spatial parameters of the stimuli. The higher thresholds for second-order stimuli may be accounted for by appealing to the properties of their noise carriers. In a study of the direction of motion in reversed-phi stimuli, it was shown that luminance and contrast defined stimuli could elicit both forwards and reversed motion. The forwards motion in the contrast defined stimulus cannot be explained by the operation of a first- or second-order channel. Perception of motion direction in the contrast defined stimulus was dependent upon the characteristics of the noise carrier. Similar dependencies were observed when noise was added to the first-order stimulus. When the effect of carrier is taken into account, both types of stimulus show similar patterns of response over spatial and temporal frequency. Modulation depth tuning curves for the detection of motion direction in stimuli where motion was defined by contrast and luminance microstructure were also investigated. Luminance microstructure can affect perceived contrast in contrast defined motion and also in static noise pattems. This implies that some early non-linearity exists in the human visual system. The filtering and rectification approach to recovery of the second-order motion should be highly effecfive at recovering the modulant. However, an estimate of the size of the non-linearity shows that only a relatively small distortion was necessary to account for the modulation depth tuning curves. The results from this thesis indicate that the carrier is crucial to the perception of second- order motion. Differences in response to first- and second-order motion may depend upon properties of the stimuli rather than the operation of separate mechanisms. It is argued that the results cast some doubt over the notion of a second-order channel. A number of alternatives are discussed