Uniform spatial pooling explains topographic organization and deviation from receptive-field scale invariance in primate V1.

Receptive field (RF) size and preferred spatial frequency (SF) vary greatly across the primary visual cortex (V1), increasing in a scale invariant fashion with eccentricity. Recent studies reveal that preferred SF also forms a fine-scale periodic map. A fundamental open question is how local variability in preferred SF is tied to the overall spatial RF. Here, we use two-photon imaging to simultaneously measure maps of RF size, phase selectivity, SF bandwidth, and orientation bandwidth-all of which were found to be topographically organized and correlate with preferred SF. Each of these newly characterized inter-map relationships strongly deviate from scale invariance, yet reveal a common motif-they are all accounted for by a model with uniform spatial pooling from scale invariant inputs. Our results and model provide novel and quantitative understanding of the output from V1 to downstream circuits.

Motion opponency in visual cortex.

Perceptual studies suggest that visual motion perception is mediated by opponent mechanisms that correspond to mutually suppressive populations of neurons sensitive to motions in opposite directions. We tested for a neuronal correlate of motion opponency using functional magnetic resonance imaging (fMRI) to measure brain activity in human visual cortex. There was strong motion opponency in a secondary visual cortical area known as the human MT complex (MT+), but there was little evidence of motion opponency in primary visual cortex. To determine whether the level of opponency in human and monkey are comparable, a variant of these experiments was performed using multiunit electrophysiological recording in areas MT and MST of the macaque monkey brain. Although there was substantial variability in the degree of opponency between recording sites, the monkey and human data were qualitatively similar on average. These results provide further evidence that: (1) direction-selective signals underly human MT+ responses, (2) neuronal signals in human MT+ support visual motion perception, (3) human MT+ is homologous to macaque monkey MT and adjacent motion sensitive brain areas, and (4) that fMRI measurements are correlated with average spiking activity.

Effect of spatial attention on the responses of area MT neurons.

This study examines the influence of spatial attention on the responses of neurons in the middle temporal visual area (MT or V5) of extrastriate cortex. Two monkeys were trained to perform a direction-discrimination task. On each trial, two apertures of random-dot stimuli appeared simultaneously at two spatially separated locations; the monkeys were required to discriminate the direction of stimulus motion at one location while ignoring the stimulus at the other location. After extensive training, we recorded the responses of MT neurons in two configurations: 1) Both apertures placed "within" the neuron's receptive field (RF) and 2) one aperture covering the RF while the other was presented at a "remote" location. For each unit we compared the responses to identical stimulus displays when the monkey was instructed to attend to one or the other aperture. The responses of MT neurons were 8.7% stronger, on average, when the monkey attended to the spatial location that contained motion in the "preferred" direction. Attentional effects were equal, on average, in the within RF and remote configurations. The attentional modulations began approximately 300 ms after stimulus onset, gradually increased throughout the trial, and peaked near stimulus offset. An analysis of the neuronal responses on error trials suggests that the monkeys failed to attend to the appropriate spatial location on these trials. The relatively weak attentional effects that we observed contrast strikingly with recent results of Treue and Maunsell, who demonstrated very strong attentional modulations (median effect >80%) in MT in a task that shares many features with ours. Our results suggest that spatial attention alone is not sufficient to induce strong attentional effects in MT even when two competing motion stimuli appear within the RF of the recorded neuron. The difference between our results and those of Treue and Maunsell suggests that the magnitude of the attentional effects in MT may depend critically on how attention is directed to a particular stimulus and on the precise demands of the task.

Color signals in area MT of the macaque monkey.

The relationship between the neural processing of color and motion information has been a contentious issue in visual neuroscience. We examined this relationship directly by measuring neural responses to isoluminant S cone signals in extrastriate area MT of the macaque monkey. S cone stimuli produced robust, direction-selective responses at most recording sites, indicating that color signals are present in MT. While these responses were unequivocal, S cone contrast sensitivity was, on average, 1.0-1.3 log units lower than luminance contrast sensitivity. The presence of S cone responses and the relative sensitivity of MT neurons to S cone and luminance signals agree with functional magnetic resonance imaging (fMRI) measurements in human MT+. The results are consistent with the hypothesis that color signals in MT influence behavior in speed judgment tasks.

Temporal gating of neural signals during performance of a visual discrimination task.

The flow of neural signals within the cerebral cortex must be subject to multiple controls as behaviour unfolds in time. In a visual discrimination task that includes a delay period, the transmission of sensory signals to circuitry that mediates memory, decision-making and motor-planning must be governed closely by 'filtering' or 'gating' mechanisms so that extraneous events occurring before, during or after presentation of the critical visual stimulus have little or no effect on the subject's behavioural responses. Here we study one such mechanism physiologically by applying electrical microstimulation to columns of directionally selective neurons in the middle temporal visual area at varying times during single trials of a direction-discrimination task. The behavioural effects of microstimulation varied strikingly according to the timing of delivery within the trial, indicating that signals produced by microstimulation may be subject to active 'gating'. Our results show several important features of this gating process: first, signal flow is modulated upwards on onset of the visual stimulus and downwards, typically with a slower time course, after stimulus offset; second, gating efficacy can be modified by behavioural training; and third, gating is implemented primarily downstream of the middle temporal visual area.

Neurophysiology: neural fingerprints of visual attention.

Pronounced effects of attention have been demonstrated in a region of visual cortex previously thought to be devoid of such influences; identifying the features critical for eliciting these effects should teach us a great deal about the neural underpinnings of visual attention.

Simultaneously recorded single units in the frontal cortex go through sequences of discrete and stable states in monkeys performing a delayed localization task.

To test whether spiking activity of six to eight simultaneously recorded neurons in the frontal cortex of a monkey can be characterized by a sequence of discrete and stable states, neuronal activity is analyzed by a hidden Markov model (HMM). Using the HMM method, we are able to detect distinct states of neuronal activity within which firing rates are approximately stationary. Transitions between states, as expressed by concomitant changes in the firing rates of several units, occur quite abruptly. The significance and consistency of the states are confirmed by comparison with simulated data. The detected states are specific to a monkey's response in a delayed localization task, allowing correct prediction of the response in approximately 90% of the trials. Similar predictive power is achieved by a model based simply on the response histograms (PSTH) of the units. The two models reach this predictive ability with different time courses: the PSTH model gains predictive power with a higher rate in the first second of the delay, and the HMM gains predictive power with higher rate in the next 3 sec. In this later period, conventional methods such as the PSTH cannot detect any firing rate modulations, but the HMM successfully captures transitions between distinct states that are specific to the monkey's behavioral response and occur at highly variable times from trial to trial. Our results suggest that neuronal activity in this later period is described best as transitions among distinct states that may reflect discrete steps in the monkey's mental processes.

Cortical activity flips among quasi-stationary states.

Parallel recordings of spike trains of several single cortical neurons in behaving monkeys were analyzed as a hidden Markov process. The parallel spike trains were considered as a multivariate Poisson process whose vector firing rates change with time. As a consequence of this approach, the complete recording can be segmented into a sequence of a few statistically discriminated hidden states, whose dynamics are modeled as a first-order Markov chain. The biological validity and benefits of this approach were examined in several independent ways: (i) the statistical consistency of the segmentation and its correspondence to the behavior of the animals; (ii) direct measurement of the collective flips of activity, obtained by the model; and (iii) the relation between the segmentation and the pair-wise short-term cross-correlations between the recorded spike trains. Comparison with surrogate data was also carried out for each of the above examinations to assure their significance. Our results indicated the existence of well-separated states of activity, within which the firing rates were approximately stationary. With our present data we could reliably discriminate six to eight such states. The transitions between states were fast and were associated with concomitant changes of firing rates of several neurons. Different behavioral modes and stimuli were consistently reflected by different states of neural activity. Moreover, the pair-wise correlations between neurons varied considerably between the different states, supporting the hypothesis that these distinct states were brought about by the cooperative action of many neurons.

Probability model for molecular recognition in biological receptor repertoires: significance to the olfactory system.

A generalized phenomenological model is presented for stereospecific recognition between biological receptors and their ligands. We ask what is the distribution of binding constants psi(K) between an arbitrary ligand and members of a large receptor repertoire, such as immunoglobulins or olfactory receptors. For binding surfaces with B potential subsite and S different types of subsite configurations, the number of successful elementary interactions obeys a binomial distribution. The discrete probability function psi(K) is then derived with assumptions on alpha, the free energy contribution per elementary interaction. The functional form of psi(K) may be universal, although the parameter values could vary for different ligand types. An estimate of the parameter values of psi(K) for iodovanillin, an analog of odorants and immunological haptens, is obtained by equilibrium dialysis experiments with nonimmune antibodies. Based on a simple relationship, predicted by the model, between the size of a receptor repertoire and its average maximal affinity toward an arbitrary ligand, the size of the olfactory receptor repertoire (Nolf) is calculated as 300-1000, in very good agreement with recent molecular biological studies. A very similar estimate, Nolf = 500, is independently derived by relating a theoretical distribution of maxima for psi(K) with published human olfactory threshold variations. The present model also has implications to the question of olfactory coding and to the analysis of specific anosmias, genetic deficits in perceiving particular odorants. More generally, the proposed model provides a better understanding of ligand specificity in biological receptors and could help in understanding their evolution.