Interactions between saccades and smooth pursuit eye movements in marmosets.

Animals use a combination of eye movements to track moving objects. These different eye movements need to be coordinated for successful tracking, requiring interactions between the systems involved. Here, we study the interaction between the saccadic and smooth pursuit eye movement systems in marmosets. Using a single target pursuit task, we show that saccades cause an enhancement in pursuit following a saccade. Using a two-target pursuit task, we show that this enhancement in pursuit is selective towards the motion of the target selected by the saccade, irrespective of any biases in pursuit prior to the saccade. These experiments highlight the similarities in the functioning of saccadic and smooth pursuit eye movement systems across primates. SIGNIFICANCE STATEMENT: We study the coordination between the smooth-pursuit and saccadic eye movement systems in marmosets using single and multiple object motions. We find that saccade to a target increases pursuit velocity towards the target. If multiple objects are visible, saccade choice makes pursuit more selective towards the saccade target. Our results show that coordination between different eye movement systems to successfully track moving objects is similar between marmosets and primates.

Primate neocortex performs balanced sensory amplification.

The sensory cortex amplifies relevant features of external stimuli. This sensitivity and selectivity arise through the transformation of inputs by cortical circuitry. We characterize the circuit mechanisms and dynamics of cortical amplification by making large-scale simultaneous measurements of single cells in awake primates and testing computational models. By comparing network activity in both driven and spontaneous states with models, we identify the circuit as operating in a regime of non-normal balanced amplification. Incoming inputs are strongly but transiently amplified by strong recurrent feedback from the disruption of excitatory-inhibitory balance in the network. Strong inhibition rapidly quenches responses, thereby permitting the tracking of time-varying stimuli.

Ocular following Eye Movements in Marmosets Follow Complex Motion Trajectories.

Ocular following eye movements help stabilize images on the retina and offer a window to study motion interpretation by visual circuits. We use these ocular following eye movements to study motion integration behavior in the marmosets. We characterize ocular following responses in the marmosets using different moving stimuli such as dot patterns, gratings, and plaids. Marmosets track motion along different directions and exhibit spatial frequency and speed sensitivity, which closely matches the sensitivity reported in neurons from their motion-selective area MT. Marmosets are also able to track the integrated motion of plaids, with tracking direction consistent with an intersection of constraints model of motion integration. Marmoset ocular following responses are similar to responses in macaques and humans with certain species-specific differences in peak sensitivities. Such motion-sensitive eye movement behavior in combination with direct access to cortical circuitry makes the marmoset model well suited to study the neural basis of motion integration.

On the Rotations of the Cranial Spheres.

We integrate information from multiple sensory modalities and from ongoing plans to construct a perception of the world. In this issue of Neuron, Bouvier et al. (2020) and Guitchounts et al. (2020) examine the detailed circuitry that supports a flexible integration of head and visual signals in rodent primary visual cortex.

Functional Access to Neuron Subclasses in Rodent and Primate Forebrain.

Viral vectors enable foreign proteins to be expressed in brains of non-genetic species, including non-human primates. However, viruses targeting specific neuron classes have proved elusive. Here we describe viral promoters and strategies for accessing GABAergic interneurons and their molecularly defined subsets in the rodent and primate. Using a set intersection approach, which relies on two co-active promoters, we can restrict heterologous protein expression to cortical and hippocampal somatostatin-positive and parvalbumin-positive interneurons. With an orthogonal set difference method, we can enrich for subclasses of neuropeptide-Y-positive GABAergic interneurons by effectively subtracting the expression pattern of one promoter from that of another. These methods harness the complexity of gene expression patterns in the brain and significantly expand the number of genetically tractable neuron classes across mammals.

Emergent Orientation Selectivity from Random Networks in Mouse Visual Cortex.

The connectivity principles underlying the emergence of orientation selectivity in primary visual cortex (V1) of mammals lacking an orientation map (such as rodents and lagomorphs) are poorly understood. We present a computational model in which random connectivity gives rise to orientation selectivity that matches experimental observations. The model predicts that mouse V1 neurons should exhibit intricate receptive fields in the two-dimensional frequency domain, causing a shift in orientation preferences with spatial frequency. We find evidence for these features in mouse V1 using calcium imaging and intracellular whole-cell recordings.

Binocular Disparity Selectivity Weakened after Monocular Deprivation in Mouse V1.

Experiences during the critical period sculpt the circuitry within the neocortex, leading to changes in the functional responses of sensory neurons. Monocular deprivation (MD) during the visual critical period causes shifts in ocular preference, or dominance, toward the open eye in primary visual cortex (V1) and disrupts the normal development of acuity. In carnivores and primates, MD also disrupts the emergence of binocular disparity selectivity, a cue resulting from integrating ocular inputs. This disruption may be a result of the increase in neurons driven exclusively by the open eye that follows deprivation or a result of a mismatch in the convergence of ocular inputs. To distinguish between these possibilities, we measured the ocular dominance (OD) and disparity selectivity of neurons from male and female mouse V1 following MD. Normal mouse V1 neurons are dominated by contralateral eye input and contralateral eye deprivation shifts mouse V1 neurons toward more balanced responses between the eyes. This shift toward binocularity, as assayed by OD, decreased disparity sensitivity. MD did not alter the initial maturation of binocularity, as disparity selectivity before the MD was indistinguishable from normal mature animals. Decreased disparity tuning was most pronounced in binocular and ipsilaterally biased neurons, which are the populations that have undergone the largest shifts in OD. In concert with the decline in disparity selectivity, we observed a shift toward lower spatial frequency selectivity for the ipsilateral eye following MD. These results suggest an emergence of novel synaptic inputs during MD that disrupt the representation of disparity selectivity.SIGNIFICANCE STATEMENT We demonstrate that monocular deprivation during the developmental critical period impairs binocular integration in mouse primary visual cortex. This impairment occurs despite an increase in the degree to which neurons become more binocular. We further demonstrate that our deprivation did not impair the maturation of disparity selectivity. Disparity selectivity has already reached a matured level before the monocular deprivation. The loss of disparity tuning is primarily observed in neurons dominated by the open eye, suggesting a link between altered inputs and loss of disparity sensitivity. These results suggest that new inputs following deprivation may not maintain the precise spatial relationship between the two eye inputs required for disparity selectivity.

Functional characterization and spatial clustering of visual cortical neurons in the predatory grasshopper mouse Onychomys arenicola.

Mammalian neocortical circuits are functionally organized such that the selectivity of individual neurons systematically shifts across the cortical surface, forming a continuous map. Maps of the sensory space exist in cortex, such as retinotopic maps in the visual system or tonotopic maps in the auditory system, but other functional response properties also may be similarly organized. For example, many carnivores and primates possess a map for orientation selectivity in primary visual cortex (V1), whereas mice, rabbits, and the gray squirrel lack orientation maps. In this report we show that a carnivorous rodent with predatory behaviors, the grasshopper mouse (Onychomys arenicola), lacks a canonical columnar organization of orientation preference in V1; however, neighboring neurons within 50 µm exhibit related tuning preference. Using a combination of two-photon microscopy and extracellular electrophysiology, we demonstrate that the functional organization of visual cortical neurons in the grasshopper mouse is largely the same as in the C57/BL6 laboratory mouse. We also find similarity in the selectivity for stimulus orientation, direction, and spatial frequency. Our results suggest that the properties of V1 neurons across rodent species are largely conserved.NEW & NOTEWORTHY Carnivores and primates possess a map for orientation selectivity in primary visual cortex (V1), whereas rodents and lagomorphs lack this organization. We examine, for the first time, V1 of a wild carnivorous rodent with predatory behaviors, the grasshopper mouse (Onychomys arenicola). We demonstrate the cellular organization of V1 in the grasshopper mouse is largely the same as the C57/BL6 laboratory mouse, suggesting that V1 neuron properties across rodent species are largely conserved.

Local Integration Accounts for Weak Selectivity of Mouse Neocortical Parvalbumin Interneurons.

Dissecting the functional roles of excitatory and inhibitory neurons in cortical circuits is a fundamental goal in neuroscience. Of particular interest are their roles in emergent cortical computations such as binocular integration in primary visual cortex (V1). We measured the binocular response selectivity of genetically defined subpopulations of excitatory and inhibitory neurons. Parvalbumin (PV+) interneurons received strong inputs from both eyes but lacked selectivity for binocular disparity. Because broad selectivity could result from heterogeneous synaptic input from neighboring neurons, we examined how individual PV+ interneuron selectivity compared to that of the local neuronal network, which is primarily composed of excitatory neurons. PV+ neurons showed functional similarity to neighboring neuronal populations over spatial distances resembling measurements of synaptic connectivity. On the other hand, excitatory neurons expressing CaMKIIα displayed no such functional similarity with the neighboring population. Our findings suggest that broad selectivity of PV+ interneurons results from nonspecific integration within local networks. VIDEO ABSTRACT.