Functional Specialization of Seven Mouse Visual Cortical Areas

SummaryTo establish the mouse as a genetically tractable model for high-order visual processing, we characterized fine-scale retinotopic organization of visual cortex and determined functional specialization of layer 2/3 neuronal populations in seven retinotopically identified areas. Each area contains a distinct visuotopic representation and encodes a unique combination of spatiotemporal features. Areas LM, AL, RL, and AM prefer up to three times faster temporal frequencies and significantly lower spatial frequencies than V1, while V1 and PM prefer high spatial and low temporal frequencies. LI prefers both high spatial and temporal frequencies. All extrastriate areas except LI increase orientation selectivity compared to V1, and three areas are significantly more direction selective (AL, RL, and AM). Specific combinations of spatiotemporal representations further distinguish areas. These results reveal that mouse higher visual areas are functionally distinct, and separate groups of areas may be specialized for motion-related versus pattern-related computations, perhaps forming pathways analogous to dorsal and ventral streams in other species

Spectrotemporal Processing in Spectral Tuning Modules of Cat Primary Auditory Cortex

Spectral integration properties show topographical order in cat primary auditory cortex (AI). Along the iso-frequency domain, regions with predominantly narrowly tuned (NT) neurons are segregated from regions with more broadly tuned (BT) neurons, forming distinct processing modules. Despite their prominent spatial segregation, spectrotemporal processing has not been compared for these regions. We identified these NT and BT regions with broad-band ripple stimuli and characterized processing differences between them using both spectrotemporal receptive fields (STRFs) and nonlinear stimulus/firing rate transformations. The durations of STRF excitatory and inhibitory subfields were shorter and the best temporal modulation frequencies were higher for BT neurons than for NT neurons. For NT neurons, the bandwidth of excitatory and inhibitory subfields was matched, whereas for BT neurons it was not. Phase locking and feature selectivity were higher for NT neurons. Properties of the nonlinearities showed only slight differences across the bandwidth modules. These results indicate fundamental differences in spectrotemporal preferences - and thus distinct physiological functions - for neurons in BT and NT spectral integration modules. However, some global processing aspects, such as spectrotemporal interactions and nonlinear input/output behavior, appear to be similar for both neuronal subgroups. The findings suggest that spectral integration modules in AI differ in what specific stimulus aspects are processed, but they are similar in the manner in which stimulus information is processed

Electrophysiological correlates of motor plans and graspability via dorsal/ventral interactions

Vision has historically been subdivided into two major systems. The vision-for-perception system is thought to be responsible for generating visual representations in service of recognition and identification. Conversely, the vision-for-action system is thought to transform visual information towards the goal of guiding motor behavior. Both systems have been linked to distinct anatomical pathways - the ventral pathway, originating in early visual cortex and terminating in the temporal lobe, is thought to mediate vision-for-perception, while the dorsal pathway, originating in early visual cortex and terminating in the parietal lobe, is thought to mediate vision-for-action. While serving as a fertile and influential theoretical framework, a growing body of evidence suggests these processing streams may not be as independent as once thought. Our current investigation is predicated on the observation that many visuomotor behaviors (mediated through the dorsal pathway), such as the manipulation of man-made tools, are contingent on the successful identification of the object (mediated through the ventral pathway). Here we investigate the nature of these interactions using High-Density Electroencephalography (HD-EEG), Multivariate Pattern analysis (MVPA) & EEG source localization. In experiment 1, participants viewed images of animate objects (birds & insects) and inanimate objects (tools & graspable objects). The frequency-tagging approach and the Fast Fourier Transform was used to examine frequency domain amplitude differences between the object categories. In experiment 2, evoked potentials from the same stimuli categories were used to explore the temporal dynamics of object processing. Next, source localization was used to explore the temporal dynamics of object processing within the dorsal and ventral pathways. Experiment 3 recapitulated the analyses used in experiment 2 on a different stimulus set (a stimulus set that controlled for the shape confound that exists between tools and graspable objects). Our results do not support the main hypothesis (i.e., we do not observe a temporal difference in the classification of tools vs. graspable objects between the dorsal and ventral pathway). Nonetheless, successful classification between the aforementioned stimulus categories is observed at the sensor level (EEG time course MVPA) as well as at the source level (source localized MVPA) in both neural pathways. These results may provide interesting implications regarding the spatiotemporal dynamics of object processing as well as the involvement of the two pathways

Pulvinar contributions to visual cortical processing in the rat

The extrageniculate visual pathway, which carries visual information from the retina through the superficial layers of the superior colliculus and the pulvinar nucleus, is poorly understood. Several studies have implicated this pathway, in particular the pulvinar, in cognitive tasks such as selective attention, but no specific mechanism or circuit has been described that could support such a function. In order to better understand what role this secondary visual pathway serves, here we examine the basic anatomical and functional properties of cells in the pulvinar, and what driving or modulating effect these cells have on visual cortex. In the first study, we made extracellular recordings in the pulvinar nucleus of lightly anesthetized rats. We identified visually responsive cells that have large receptive fields on the order of 80 degrees of visual field, fire selectively in response to low spatial frequencies, and can sometimes be selective to the direction or orientation of moving grating stimuli. We also determined that the anatomically-defined lateral subdivision encodes a greater diversity of temporal frequency stimuli than the more medial subdivision, which has better direction selectivity. In the second study, we used modified rabies viruses to retrogradely trace connections between rat pulvinar and visual cortex in order to better understand from where pulvinar receives its visual information and to which cortical areas it is best connected. We found a significantly weaker projection from pulvinar to primary visual cortex (V1) than from pulvinar to higher visual cortex (V2). In the final study, we designed and tested a new modified rabies virus to optically excite and silence populations of the more numerous projections to V2 from the rat pulvinar. We found that pulvinar modulates cortical size tuning and suppresses flash responses, but doesn’t drive activity in V2. This dissertation builds a foundational understanding of the role of the pulvinar nucleus in rodents, illustrating how pulvinar integrates spatiotemporal information from visual cortex and the superior colliculus, and regulates firing rates in rodent V2. The new rabies virus variant described here is well suited to test theories of pulvinar function, in addition to its wide potential applications in non-transgenic animals such as cats or non-human primates, where models of pulvinar are already well developed

Integrating Spatial Working Memory and Remote Memory: Interactions between the Medial Prefrontal Cortex and Hippocampus

In recent years, two separate research streams have focused on information sharing between the medial prefrontal cortex (mPFC) and hippocampus (HC). Research into spatial working memory has shown that successful execution of many types of behaviors requires synchronous activity in the theta range between the mPFC and HC, whereas studies of memory consolidation have shown that shifts in area dependency may be temporally modulated. While the nature of information that is being communicated is still unclear, spatial working memory and remote memory recall is reliant on interactions between these two areas. This review will present recent evidence that shows that these two processes are not as separate as they first appeared. We will also present a novel conceptualization of the nature of the medial prefrontal representation and how this might help explain this area’s role in spatial working memory and remote memory recall

Functional Specialization of eye-specific visual pathways into higher visual cortex

The brain is able to construct a visual representation of the world by parallel processing of cortical neurons that prefer increasingly complex stimuli. One way the visual cortex has accomplished parallel processing is by creating functionally organized modules that are tuned to unique features and linking them in multiple processing stages of cortex. For example, primary visual cortex (V1) sends functionally distinct information to higher visual areas (HVAs), which are more specialized in their processing of spatiotemporal information. Inherently coupled to this process is the convergence of eye-specific inputs in visual cortex. Shifting the eye-specific tuning of neurons in primary visual cortex by monocular deprivation in early life is known to disrupt tuning for spatial frequency in adulthood. Combining space and time better characterizes the segregation of HVAs. To begin to understand if eye-specific responses could be linked to tuning properties important for the segregation of HVAs, we characterized eye-specific spatiotemporal tuning of layer 2/3 excitatory cells within the binocular zone of V1 and two HVAs grouped into the putative ventral and dorsal streams, LM and PM, using two-photon GCaMP6s imaging of awake mice. An asymmetry was found at the level of V1, such that responses driven primarily by the contralateral eye were biased towards high spatial frequencies, low speeds, cardinal directions, and were more direction selective than binocular or ipsilateral eye-driven responses. Eye-specific inputs in V1 are tuned to different speeds and also have different degrees of speed tuning, where contralateral eye inputs are more speed tuned than ipsilateral eye inputs. The proportions of eye-specific neurons of LM and PM matched the expected preferences based on eye-specific spatial frequency tuning found at the level of V1. A similar contralateral bias for distinct features, most notably, spatiotemporal tuning, was found within LM and PM, linking neurons with similar eye-specific preferences to their tuning for early feature detectors important for stream specialization. To determine if V1 sends eye-specific functionally distinct information to HVAs, we injected AAV-Syn-GCaMP6s into the binocular zone of V1 and imaged the afferents that targeted either LM or PM. We found that V1 afferents to LM and PM were distinct in their distributions for ocular dominance, suggesting that eye-specific projections from V1 to HVAs contribute to their functional specificity. To determine if the functional specialization of HVAs depend upon eye-specific developmental mechanisms, we deprived mice of visual experience through the contralateral eye (CMD) during the ocular dominance critical period and assessed eye-specific spatiotemporal tuning of V1, LM and PM in adulthood. We found that CMD diminished the functional specificity of V1, LM and PM, resulting in areas without differentiated spatiotemporal preferences. Moreover, the eye-specific functional segregation was also disrupted with CMD. Altogether, our data demonstrates that the maturation of higher visual areas is dependent on proper binocular visual experience and suggests that the functional specialization of eye-specific responses could be an efficient routing mechanism to differentiate higher visual areas

Organization of the dorsal lateral geniculate nucleus in the mouse

AbstractThe dorsal lateral geniculate nucleus (dLGN) of the thalamus is the principal conduit for visual information from retina to visual cortex. Viewed initially as a simple relay, recent studies in the mouse reveal far greater complexity in the way input from the retina is combined, transmitted, and processed in dLGN. Here we consider the structural and functional organization of the mouse retinogeniculate pathway by examining the patterns of retinal projections to dLGN and how they converge onto thalamocortical neurons to shape the flow of visual information to visual cortex.</jats:p

The Influence of the Dorsal Pathway on Enhanced Visual Processing

Overall our visual experience is such a seamless one that unless specifically told, we might never know that what we see is actually the visual system taking the very simple input provided by cells in the retina and constructing an image based on rules and calculations and algorithms neuroscientists have yet to fully uncover. This is an incredible feat given the plethora of visual stimuli within our environment, that this information is used to inform and plan actions, and if that wasnt enough, the visual system also has the capacity to selectively enhance certain aspects of visual processing if needs be. The research contained within this dissertation seeks to investigate how the dorsal visual pathway enhances both decision-making processes and visual stimuli presented near the hand. Our findings suggest that the formation of object representations in the dorsal pathway can include both ventral (colour, contrast) and dorsal (speed) stream features (chapters two and three), which in turn greatly speed decision-making processes within the dorsal pathway. In addition, contrast and speed are integrated automatically but purely ventral stream features, such as colour, require top-down attention to facilitate enhanced processing speeds (chapter three). In chapter four we find that visual processing near the hand is enhanced in a novel way. When the hand is nearby, orientation tuning is sharpened in a manner not consistent with either oculomotor-driven spatial or feature based attention. In addition, response variability is reduced when the hand is nearby, raising the possibility that enhanced processing near the hand maybe be driven by feedback from frontoparietal reaching and grasping regions. The research within this dissertation includes important new information regarding how the dorsal pathway can speed visual processing, and provides insight as to the next stage in understanding how we use vision for action