Maureen A. Hagan

Only Coherent Spiking in Posterior Parietal Cortex Coordinates Looking and Reaching

Here, we report that temporally patterned, coherent spiking activity in the posterior parietal cortex (PPC) coordinates the timing of looking and reaching. Using a spike-field approach, we identify a population of parietal area LIP neurons that fire spikes coherently with 15 Hz beta-frequency LFP activity. The firing rate of coherently active neurons predicts the reaction times (RTs) of coordinated reach-saccade movements but not of saccades when made alone. Area LIP neurons that do not fire coherently do not predict RT of either movement type. Similar beta-band LFP activity is present in the parietal reach region but not nearby visual area V3d. This suggests that coherent spiking activity in PPC can control reaches and saccades together. We propose that the neural mechanism of coordination involves a shared representation that acts to slow or speed movements together.

Spike-field activity in parietal area LIP during coordinated reach and saccade movements

The posterior parietal cortex is situated between visual and motor areas and supports coordinated visually guided behavior. Area LIP in the intraparietal sulcus contains representations of visual space and has been extensively studied in the context of saccades. However, area LIP has not been studied during coordinated movements, so it is not known whether saccadic representations in area LIP are influenced by coordinated behavior. Here, we studied spiking and local field potential (LFP) activity in area LIP while subjects performed coordinated reaches and saccades or saccades alone to remembered target locations to test whether activity in area LIP is influenced by the presence of a coordinated reach. We find that coordination significantly changes the activity of individual neurons in area LIP, increasing or decreasing the firing rate when a reach is made with a saccade compared with when a saccade is made alone. Analyzing spike-field coherence demonstrates that area LIP neurons whose firing rate is suppressed during the coordinated task have activity temporally correlated with nearby LFP activity, which reflects the synaptic activity of populations of neurons. Area LIP neurons whose firing rate increases during the coordinated task do not show significant spike-field coherence. Furthermore, LFP power in area LIP is suppressed and does not increase when a coordinated reach is made with a saccade. These results demonstrate that area LIP neurons display different responses to coordinated reach and saccade movements, and that different spike rate responses are associated with different patterns of correlated activity. The population of neurons whose firing rate is suppressed is coherently active with local populations of LIP neurons. Overall, these results suggest that area LIP plays a role in coordinating visually guided actions through suppression of coherent patterns of saccade-related activity.

Neural plasticity following lesions of the primate occipital lobe: The marmoset as an animal model for studies of blindsight.

For nearly a century it has been observed that some residual visually guided behavior can persist after damage to the primary visual cortex (V1) in primates. The age at which damage to V1 occurs leads to different outcomes, with V1 lesions in infancy allowing better preservation of visual faculties in comparison with those incurred in adulthood. While adult V1 lesions may still allow retention of some limited visual abilities, these are subconscious—a characteristic that has led to this form of residual vision being referred to as blindsight. The neural basis of blindsight has been of great interest to the neuroscience community, with particular focus on understanding the contributions of the different subcortical pathways and cortical areas that may underlie this phenomenon. More recently, research has started to address which forms of neural plasticity occur following V1 lesions at different ages, including work using marmoset monkeys. The relatively rapid postnatal development of this species, allied to the lissencephalic brains and well‐characterized visual cortex provide significant technical advantages, which allow controlled experiments exploring visual function in the absence of V1.

Linking structure and function: Development of lateral spatial interactions in macaque monkeys

Lateral spatial interactions among elements of a scene, which either enhance or degrade visual performance, are ubiquitous in vision. The neural mechanisms underlying lateral spatial interactions are a matter of debate, and various hypotheses have been proposed. Suppressive effects may be due to local inhibitory interactions, whereas facilitatory effects are typically ascribed either to the function of long-range horizontal projections in V1 or to uncertainty reduction. We investigated the development of lateral spatial interactions, facilitation and suppression, and compared their developmental profiles to those of potential underlying mechanisms in the visual system of infant macaques. Animals ranging in age from 10 weeks to 3 years were tested with a lateral masking paradigm. We found that suppressive interactions are present from very early in postnatal life, showing no change over the age range tested. However, facilitation develops slowly over the first year after birth. Our data suggest that the early maturation of suppressive interactions is related to the relatively mature receptive field properties of neurons in early visual cortical areas near birth in infant macaques, whereas the later maturation of facilitation is unlikely to be explained by development of local or long-range connectivity in primary visual cortex. Instead our data favor a late developing feedback or top-down cognitive process to explain the origin of facilitation.

Auditory motion does not modulate spiking activity in the middle temporal and medial superior temporal visual areas

The integration of multiple sensory modalities is a key aspect of brain function, allowing animals to take advantage of concurrent sources of information to make more accurate perceptual judgments. For many years, multisensory integration in the cerebral cortex was deemed to occur only in high‐level “polysensory” association areas. However, more recent studies have suggested that cross‐modal stimulation can also influence neural activity in areas traditionally considered to be 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 audiovisual 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 audiovisual 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.

Spatially dynamic recurrent information flow across long‐range dorsal motor network encodes selective motor goals

Performing voluntary movements involves many regions of the brain, but it is unknown how they work together to plan and execute specific movements. We recorded high‐resolution ultra‐high‐field blood‐oxygen‐level‐dependent signal during a cued ankle‐dorsiflexion task. The spatiotemporal dynamics and the patterns of task‐relevant information flow across the dorsal motor network were investigated. We show that task‐relevant information appears and decays earlier in the higher order areas of the dorsal motor network then in the primary motor cortex. Furthermore, the results show that task‐relevant information is encoded in general initially, and then selective goals are subsequently encoded in specifics subregions across the network. Importantly, the patterns of recurrent information flow across the network vary across different subregions depending on the goal. Recurrent information flow was observed across all higher order areas of the dorsal motor network in the subregions encoding for the current goal. In contrast, only the top–down information flow from the supplementary motor cortex to the frontoparietal regions, with weakened recurrent information flow between the frontoparietal regions and bottom–up information flow from the frontoparietal regions to the supplementary cortex were observed in the subregions encoding for the opposing goal. We conclude that selective motor goal encoding and execution rely on goal‐dependent differences in subregional recurrent information flow patterns across the long‐range dorsal motor network areas that exhibit graded functional specialization.

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

The effect of temporal correlations in the activity of sensory neurons remains a subject of debate, with some studies suggesting that correlations may be detrimental to population coding (by reducing the amount of information that can be extracted) or may actually enhance population coding. The study of neuronal responses to random-dot motion patterns has provided the some of the most valuable insights into how the activity of neurons is related to perception. However, it is currently unknown how changes in the strength of motion signals, through the reduction of coherence of random dot patterns, affects correlated activity and population decoding. To address this question, 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. We used the spike rates of simultaneously recorded neurons to decode the direction of motion at each level of coherence using linear classifiers. We found that reducing motion coherence increased neuronal correlations, yet the correlation structure was conserved. We also found that removing correlations with trial shuffling generally improved population decoding performance and ignoring correlations generally impaired decoding performance. Finally, we showed that decoders trained at 100% coherence have similar performance to decoders optimized for each level of coherence, demonstrating that the optimal linear readout is independent of coherence. These results have implications for how information is encoded by populations of neurons, as well as how they may be decoded by downstream areas in decision making tasks.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. Significance Statement Many 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.

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.

Feasibility of identifying the ideal locations for motor intention decoding using unimodal and multimodal classification at 7T-fMRI

Invasive Brain-Computer Interfaces (BCIs) require surgeries with high health-risks. The risk-to-benefit ratio of the procedure could potentially be improved by pre-surgically identifying the ideal locations for mental strategy classification. We recorded high-spatiotemporal resolution blood-oxygenation-level-dependent (BOLD) signals using functional MRI at 7 Tesla in eleven healthy participants during two motor imagery tasks. BCI diagnostic task isolated the intent to imagine movements, while BCI simulation task simulated the neural states that may be yielded in a real-life BCI-operation scenario. Imagination of movements were classified from the BOLD signals in sub-regions of activation within a single or multiple dorsal motor network regions. Then, the participant’s decoding performance during the BCI simulation task was predicted from the BCI diagnostic task. The results revealed that drawing information from multiple regions compared to a single region increased the classification accuracy of imagined movements. Importantly, systematic unimodal and multimodal classification revealed the ideal combination of regions that yielded the best classification accuracy at the individual-level. Lastly, a given participant’s decoding performance achieved during the BCI simulation task could be predicted from the BCI diagnostic task. These results show the feasibility of 7T-fMRI with unimodal and multimodal classification being utilized for identifying ideal sites for mental strategy classification.

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.