Biology subjects

Hagan, M. A.

Publications and source records attributed to Hagan, M. A..

12 recordsLinked to original sources

bioRxiv2026

Speed judgments during smooth pursuit reflect low gain efference copy

During smooth pursuit eye movements, the visual system must compensate for self-generated retinal motion to achieve stable perception of motion in the environment. This compensation primarily depends on an efferent copy of motor commands. Systematically under- or overweighting the strength of efference copy should lead to correlations between eye movement velocity and perceived object velocity. However, previous examinations of these trial-by-trial perceptual correlations have produced mixed results. It remains unclear how effectively the brain compensates for eye movement induced retinal motion during pursuit, and what this reveals about the way efference copy influences perception. To address this, we developed a speed perturbation paradigm in which 29 participants tracked a moving target that underwent brief speed changes. On each trial, we recorded eye velocity along with perceptual judgments of the sign of the speed change (faster or slower) and confidence ratings for those judgments. Across participants, perceptual and oculomotor sensitivity were correlated (r =0.53), but trial-by-trial perceptual and oculomotor responses appeared independent. A logistic regression model incorporating efference copy gain to predict perceptual reports from stimulus speed and eye speed revealed systematic under-compensation for eye movements; faster eye movements were associated with lower changes in perceived speed. Confidence ratings were well-calibrated to perceptual accuracy and showed a consistent negative relationship with eye movement speed. Collectively, these results are consistent with systematic under compensation for eye movements through the use of efference copy during motion perception.

physiology↗

bioRxiv2026

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↗

bioRxiv2025

Model-based separation of visual and oculomotor signals in marmoset lateral intraparietal area

The lateral intraparietal area (LIP) integrates visual information with task demands to guide saccadic eye movements. Most prior studies have relied on imposed prolonged delays to separate sensory and motor activity, whereas natural behavior involves rapid sensory-motor transformations. To examine LIP function during more naturalistic oculomotor behavior, we recorded multi-unit activity from LIP in two marmosets performing a task requiring rapid selection of salient visual stimuli. Because sensory and motor signals temporally overlap in such fast tasks, we used a Generalized Linear Model (GLM) that separately captured visually driven and oculomotor-related components. The model explained substantial neural variance during correct and missed saccades, as well as spontaneous eye movements, and revealed heterogeneous sensory and motor encoding across recorded neural units. Our approach demonstrated that the origins of neural activity can be segregated without relying on imposed delays, and showed the presence of a strong post-saccadic motor signal in LIP.

neuroscience↗

bioRxiv2023

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↗

bioRxiv2022

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↗

bioRxiv2020

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↗

bioRxiv2020

Functional inhibition across a visuomotor communication channel coordinates looking and reaching

Looking and reaching are controlled by different brain regions and coordinated during natural behaviour1-3. Understanding how flexible, natural behaviours like coordinated looking-and-reaching are controlled depends on understanding how neurons in different regions of the brain communicate4. Excitatory multiregional communication recruits neural coherence in a gamma-frequency (40-90 Hz) band5. Inhibitory control mechanisms are also required to flexibly control behaviour6, but little is known about how neurons in one region transiently suppress individual neurons in another to support behaviour. How does neuronal firing in a sender-region transiently suppress firing in a receiver-region? Here, we study inhibitory communication during a flexible, natural behaviour, termed gaze-anchoring, in which saccades are transiently inhibited by coordinated reaches. During gaze-anchoring, we find that neurons in the reach region of the posterior parietal cortex can inhibit neuronal firing in the parietal saccade region to suppress eye movements and improve reach accuracy. Importantly, suppression is transient, only present around the coordinated reach, and greatest when reach neurons fire spikes at a particular phase of beta-frequency (15-25 Hz) activity, not gamma-frequency activity. Our work provides evidence in the activity of single neurons for a novel mechanism of inhibitory communication in which beta-frequency neural coherence transiently inhibits multiregional communication to flexibly coordinate our natural behaviour.

neuroscience↗

bioRxiv2018

Coherent neuronal dynamics driven by optogenetic stimulation in the primate brain

Coherent neuronal dynamics play an important role in complex cognitive functions. Optogenetic stimulation promises to provide new ways to test the functional significance of coherent neural activity. However, the mechanisms by which optogenetic stimulation drives coherent dynamics remain unclear, especially in the non-human primate brain. Here, we perform computational modeling and experiments to study the mechanisms of optogenetic-stimulation-driven coherent neuronal dynamics in non-human primates. Neural responses arise from stimulation-evoked temporal windows of excitatory and inhibitory activity. The temporal properties of the E-I windows generate coherent neuronal dynamics at varied frequencies and depend on optogenetic stimulation parameters. Experimental results agree with parameter dependent predictions from the computational models. These results demonstrate that responses to optogenetic stimulation are governed by local circuit properties that alter the timing of E-I activity. Transient imbalances in excitatory and inhibitory activity may provide a general mechanism for generating coherent neuronal dynamics.

neuroscience↗

bioRxiv2018

Removing neural correlations improves population sensitivity in MT/MST in response to random dot stimuli

The study of neuronal responses to random-dot motion patterns has provided some of the most valuable insights into how the activity of neurons is related to perception. In the opposite directions of motion paradigm, the motion signal strength is decreased by manipulating the coherence of random dot patterns to examine how well the activity of single neurons represents the direction of motion. To extend this paradigm to populations of neurons, studies have used modelling based on data from pairs of neurons, but several important questions require further investigation with larger neuronal datasets. We recorded neuronal populations in the middle temporal (MT) and medial superior temporal (MST) areas of anaesthetized marmosets with electrode arrays, while varying the coherence of random dot patterns in two opposite directions of motion (left and right). Using the spike rates of simultaneously recorded neurons, we decoded the direction of motion at each level of coherence with linear classifiers. We found that the presence of correlations had a detrimental effect to decoding performance, but that learning the correlation structure produced better decoding performance compared to decoders that ignored the correlation structure. We also found that reducing motion coherence increased neuronal correlations, but decoders did not need to be optimized for each coherence level. Finally, we showed that decoder weights depend of left-right selectivity at 100% coherence, rather than the preferred direction. These results have implications for understanding how the information encoded by populations of neurons is affected by correlations in spiking activity.\n\nSignificance StatementMany studies have examined how the spiking activity of single neurons can encode stimulus features, such the direction of motion of visual stimuli. However, majority of such studies to date have only recorded from a small number of neurons at the same time, meaning that one cannot adequately account for the trial-to-trial correlations in spiking activity between neurons. Using multi-channel recordings, we were able to measure the neuronal correlations, and their effects on population coding of stimulus features. Our results have implications on the way which neural populations must be readout in order to maximize information.

neuroscience↗

bioRxiv2017

Altered sensitivity to motion of area MT neurons following long-term V1 lesions

The middle temporal area (MT) receives its main afferents from the striate cortex (V1). However, MT also receives direct thalamic projections, which have been hypothesized to play a crucial role in residual vision after V1 lesions. MT neurons continue to respond shortly after V1 lesions, but human clinical work has shown that lesion effects can take up to six months to stabilize, making it important to understand MT responses after long-term deprivation of V1 inputs. We recorded neuronal responses in MT to moving dot stimuli in adult marmoset monkeys, 7-11 months after unilateral V1 lesions. Fewer MT neurons were direction selective, including neurons whose locations corresponded to the intact parts of V1. Firing rates were higher and more variable, and increased with motion strength regardless of direction. These properties could be re-created by a network model with imbalanced inhibition and excitation, providing the first insights into functional implications of long-term plasticity in MT following V1 lesions.

neuroscience↗

bioRxiv2017

Auditory motion does not modulate spiking activity in visual motion processing areas MT and MST

The integration of multiple sensory modalities is one of the key aspects of brain function, allowing animals to take advantage of concurrent sources of information to make more accurate perceptual judgments. For many years, it was thought that multisensory integration in the cerebral cortex only occurs in high-level \"polysensory\" association areas, but recent studies have demonstrated cross-modal influences in regions that were traditionally designated as unimodal. In particular, several human neuroimaging studies have reported that extrastriate areas involved in visual motion perception are also activated by auditory motion, and may integrate audio-visual motion cues. However, the exact nature and extent of the effects of auditory motion on the visual cortex have not been studied at the single neuron level. We recorded the spiking activity of neurons in the middle temporal (MT) and medial superior temporal (MST) areas of anesthetized marmoset monkeys upon presentation of unimodal stimuli (moving auditory or visual patterns), as well as bimodal stimuli (concurrent audio-visual motion). Despite robust, direction selective responses to visual motion, none of the sampled neurons responded to auditory motion stimuli. Moreover, concurrent moving auditory stimuli had no significant effect on the ability of single MT and MST neurons, or populations of simultaneously recorded neurons, to discriminate the direction of motion of visual stimuli (moving random dot patterns with varying levels of motion noise). Our findings do not support the hypothesis that direct interactions between MT, MST and areas low in the hierarchy of auditory areas underlie audiovisual motion integration.\n\nSignificance StatementMany studies have demonstrated that brain regions originally thought to be unisensory may play a role in multisensory processing. For example, some neuroimaging studies have found activity in regions involved in the processing of visual motion can be modified by auditory motion. We tested whether the spiking activity of neurons in two visual motion processing areas of the primate brain, areas MT and MST, can be modulated by moving auditory stimuli. Our results revealed that neurons in these areas neither respond to auditory motion, nor change their responses to visual motion according to auditory motion along the frontoparallel plane. These findings call into question the idea that audio-visual integration occurs at early stages of processing in the extrastriate cortex.

neuroscience↗

bioRxiv2017

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↗