Search bioRxiv⌕ Search

Biology subjects

Price, N. S. C.

Publications and source records attributed to Price, N. S. C..

8 recordsLinked to original sources

Sensory origin of oculomotor variability revealed by MT population activity

Motor outputs vary even in response to identical sensory inputs, yet the origin of this variability within the sensorimotor pathway remains unresolved. Here, we evaluate how variability in sensory representations can explain behavioural fluctuations in a reflexive oculomotor task. We used Neuropixels probes to record neuronal activity in area MT of marmosets during ocular following responses and applied partial least squares regression to extract the shared variance between population activity and eye movements. Stimulus-evoked activity reliably predicted trial-by-trial variability in open-loop eye velocity. Additionally, closed-loop analyses revealed trial-by-trial correspondence between eye movements and subsequent neural responses. These results demonstrate that variability in sensory neural populations contributes to motor variability, supporting the claim that sensory noise is propagated through the sensorimotor pathway. Surprisingly, however, traditional models trained to only capture neural variability across trials poorly predicted behavioural variations, suggesting that only a subset of sensory representations is accessible to the motor system.

neuroscience↗

Naturalistic Movies and Encoding Analysis Redefine Areal Borders in Primate Visual Cortex

Accurate definition of the borders of cortical visual areas is essential for the study of neuronal processes leading to perception. However, data used for definition of areal boundaries has suffered from issues related to resolution, uniform coverage, or suitability for objective analysis, leading to ambiguity. Here, we present a novel approach that combines widefield optical imaging, presentation of naturalistic movies, and encoding model analysis, to objectively define borders in the primate extrastriate cortex. We applied this method to test conflicting hypotheses about the third-tier visual cortex, where areal boundaries have remained controversial. The results support a hypothesis whereby an area contains representations of both the upper and lower contralateral quadrants (DM) is located immediate anterior to V2, and unveil pronounced tuning preferences in the third-tier areas. High-density electrophysiological recordings with a Neuropixels probe confirm these findings. Our encoding-model approach offers a powerful, objective way to disambiguate areal boundaries.

neuroscience↗

Ocular following responses of the marmoset monkey are dependent on post-saccadic delay, spatiotemporal frequency and saccade direction

Ocular following is a short-latency, reflexive eye movement that tracks wide-field visual motion. It has been studied extensively in humans and macaques and is an appealing behaviour for studying sensory-motor transformations in the brain due to its rapidity and rigidity. We explored ocular following in the marmoset, an emerging model in neuroscience because their lissencephalic brain allows direct access to most cortical areas for imaging and electrophysiological recordings. In three experiments, we tested ocular following responses in three adult marmosets. First, we varied the gap between saccade end and stimulus motion onset (post-saccadic delay), from 10 to 300 ms. As in other species, tracking had shorter onset latencies and higher eye speeds with shorter post-saccadic delays. Second, using sine-wave grating stimuli we explored the dependence of eye speed on spatiotemporal frequency. The highest eye speed was evoked at [~]16 Hz and [~]0.16 cycles per degree (cpd), however, the highest gain was elicited at [~]1.6 Hz and [~]1.2 cpd. The highest eye speed for each spatial frequency was observed at a different temporal frequency, but this interdependence was not consistent with complete speed tuning of the ocular following response. Finally, we found the highest eye speeds when saccade and stimulus motion directions were congruent, although latencies were unaffected by direction congruence. Our results showed comparable ocular following in marmosets, humans and macaques, despite over an order of magnitude variation in body and eye size across species. This characterization will help future studies examining the neural basis of sensory-motor transformations. New & NoteworthyPrevious ocular following studies focused on humans and macaques. We examined the properties of ocular following responses in marmosets in three experiments, in which post-saccadic delay, spatial-temporal frequency of stimuli and congruency of saccade and motion directions were manipulated. We have demonstrated short-latency ocular following in marmosets, and discuss the similarities across three species that vary markedly in eye and head size. Our findings will help future studies examining the neural mechanism of sensory-motor transformations.

neuroscience↗

Neural responses to broadband visual flicker in marmoset primary visual cortex

Temporal information is ubiquitous in natural vision and must be represented accurately in the brain to allow us to interact with a constantly changing world. Recent studies have employed a random stimulation paradigm to map the temporal response function (TRF) to luminance changes in the human EEG. This approach has revealed that the visual system, when presented with broadband visual input, actively selects distinct temporal frequencies, and retains their phase-information for prolonged periods of time. This non-linear response likely originates in primary visual cortex (V1), yet, so far it has not been investigated on a neural level. Here, we characterize the steady-state response to random broadband visual flicker in marmoset V1. In two experiments, we recorded from i) marmosets passively stimulated under general anesthesia, and ii) awake marmosets, under free viewing conditions. Our results show that LFP coupling to the stimulus was broadband and unselective under anesthesia, whereas in awake animals, it was restricted to two distinct frequency components, in the alpha and beta range. Within these frequency bands, coupling adhered to the receptive field (RF) boundaries of the local populations. The responses outside the RF did not provide evidence for a propagation of stimulus information across the cortex, contrary to results in human EEG studies. This result may be explained by short fixation durations, warranting further investigation. In summary, our findings show that during awake behavior V1 neural responses to broadband information are selective for distinct frequency bands, and that this selectivity is likely controlled actively by top-down mechanisms.

neuroscience↗

Long-range neural coherence encodes stimulus information in primate visual cortex

In the primary visual cortex, neurons with similar receptive field properties are bound together through widespread networks of horizontal connections that span orientation columns. How connectivity across the cortical surface relates to stimulus information is not fully understood. We recorded spiking activity and the local field potential (LFP) from the primary visual cortex of marmoset monkeys and examined how connectivity between distant orientation columns affect the encoding of visual orientation. Regardless of their spatial separation, recording sites with similar orientation preferences have higher coherence between spiking activity and the local field potential than sites with different preferred orientation. Using information theoretic methods, we measured the amount of stimulus information that is shared between pairs of sites. More stimulus information can be decoded from pairs with the same preferred stimulus orientation than the pairs with a different preferred orientation, and the amount of information is significantly correlated with the magnitude of beta-band spike-LFP coherence. These effects remained after controlling for firing rate differences. Our results thus show that spike-LFP synchronization in the beta-band is associated with the encoding of stimulus information within the primary visual cortex of marmoset monkeys. Significance StatementA fundamental step in processing images in the visual cortex is coordinating the neural activity across distributed populations of neurons. Here, we demonstrate that populations of neurons in the primary visual cortex of marmoset monkeys with the same stimulus orientation preference temporally coordinate their activity patterns when presented with a visual stimulus. We find maximum synchronization in the beta range depends on the similarity of orientation preference at each pair of the neural population.

neuroscience↗

A \"twisted\" visual field map in the primate cortex predicted by topographic continuity

Adjacent neurons in visual cortex have overlapping receptive fields within and across area boundaries, an arrangement which is theorized to minimize wiring cost. This constraint is thought to create retinotopic maps of opposing field sign (mirror and non-mirror representations of the visual field) in adjacent visual areas, a concept which has become central in current attempts to subdivide the cortex. We modelled a realistic developmental scenario in which adjacent areas do not mature simultaneously, but need to maintain topographic continuity across their borders. This showed that the same mechanism that is hypothesized to maintain topographic continuity within each area can lead to a more complex type of retinotopic map, consisting of sectors with opposing field sign within a same area. Using fully quantitative electrode array recordings, we then demonstrate that this type of map exists in the primate extrastriate cortex.

neuroscience↗

The most informative neural code accounts for population heterogeneity

Perception is produced by reading out the representation of a sensory stimulus contained in the firing rates of a population of neurons. To examine experimentally how populations code information, a common approach is to decode a linearly-weighted sum of the neurons firing rates. This approach is popular because of its biological validity: weights in a computational decoder are analogous to synaptic strengths. For neurons recorded in vivo, weights are highly variable when derived through machine learning methods, but it is unclear what neuronal properties explain this variability, and how the variability affects decoding performance. To address this, we recorded from neurons in the middle temporal area (MT) of anesthetized marmosets (Callithrix jacchus) viewing stimuli comprising a sheet of dots that moved coherently in one of twelve different directions. We found that high gain and direction selectivity both predicted that a neuron would be weighted more highly in an optimised decoding model. Although learned weights differed markedly from weights chosen according to a priori rules based on a neurons tuning profile, decoding performance was only marginally better for the learned weights. In the models with a priori rules, selectivity is the best predictor of weighting, and defining weights according to a neurons preferred direction and selectivity improves decoding performance to very near the maximum level possible, as defined by the learned weights.\n\nNew & NoteworthyWe examined which aspects of a neurons tuning account for its contribution to sensory coding. Strongly direction-selective neurons were weighted most highly by machine learning algorithms trained to discriminate motion direction. Models with a priori defined decoding weights demonstrate that the learned weighting scheme causally improved direction representation by a neuronal population. Optimising decoders (using machine learning) lead to only marginally better performance than decoders based purely on a neurons preferred direction and selectivity.

neuroscience↗

Sensitivity of Neurons in the Middle Temporal Area of Marmoset Monkeys to Random Dot Motion

Neurons in the Middle Temporal area (MT) of the primate cerebral cortex respond to moving visual stimuli. The sensitivity of MT neurons to motion signals can be characterized by using random-dot stimuli, in which the strength of the motion signal is manipulated by adding different levels of noise (elements that move in random directions). In macaques, this has allowed the calculation of \"neurometric\" thresholds. We characterized the responses of MT neurons in sufentanil/nitrous oxide anesthetized marmoset monkeys, a species which has attracted considerable recent interest as an animal model for vision research. We found that MT neurons show a wide range of neurometric thresholds, and that the responses of the most sensitive neurons could account for the behavioral performance of macaques and humans. We also investigated factors that contributed to the wide range of observed thresholds. The difference in firing rate between responses to motion in the preferred and null directions was the most effective predictor of neurometric threshold, whereas the direction tuning bandwidth had no correlation with the threshold. We also showed that it is possible to obtain reliable estimates of neurometric thresholds using stimuli that were not highly optimized for each neuron, as is often necessary when recording from large populations of neurons with different receptive field concurrently, as was the case in this study. These results demonstrate that marmoset MT shows an essential physiological similarity to macaque MT, and suggest that its neurons are capable of representing motion signals that allow for comparable motion-in-noise judgments.\n\nNew and NoteworthyWe report the activity of neurons in marmoset MT in response to random-dot motion stimuli of varying coherence. The information carried by individual MT neurons was comparable to that of the macaque, and that the maximum firing rates were a strong predictor of sensitivity. Our study provides key information regarding the neural basis of motion perception in the marmoset, a small primate species that is becoming increasingly popular as an experimental model.

neuroscience↗