Physiological Studies on Neural Mechanisms of Visual Localization and Discrimination*

The retinotopic map depicts the cortical neurons’ response to visual stimuli on the retina and has contributed significantly to our understanding of human visual system. Although recent advances in high field functional magnetic resonance imaging (fMRI) have made it possible to generate the in vivo retinotopic map with great detail, quantifying the map remains challenging. Existing quantification methods do not preserve surface topology and often introduce large geometric distortions to the map. In this study, we developed a new framework based on computational conformal geometry and quasiconformal Teichmüller theory to quantify the retinotopic map. Specifically, we introduced a general pipeline, consisting of cortical surface conformal parameterization, surface-spline-based cortical activation signal smoothing, and vertex-wise Beltrami coefficient-based map description. After correcting most of the violations of the topological conditions, the result was a “Beltrami coefficient map” (BCM) that rigorously and completely characterizes the retinotopic map by quantifying the local quasiconformal mapping distortion at each visual field location. The BCM provided topological and fully reconstructable retinotopic maps. We successfully applied the new framework to analyze the V1 retinotopic maps from the Human Connectome Project (n=181), the largest state of the art retinotopy dataset currently available. With unprecedented precision, we found that the V1 retinotopic map was quasiconformal and the local mapping distortions were similar across observers. The new framework can be applied to other visual areas and retinotopic maps of individuals with and without eye diseases, and improve our understanding of visual cortical organization in normal and clinical populations.

We begin with the functions of the striate cortex (area V1 of the visual cortex) and end with a review of the effects of damage to striate cortex or its inputs; namely, homonymous hemifield defects. Clinical and anatomical studies accrued over the past 25 years have modified our understanding of the role of V1 in vision. We discuss the evidence that V1 is not the sole recipient of visual signals; is not the earliest recipient of visual signals; and is not essential for conscious vision. In the second section, we give a brief history of how the visual field was found to be represented in striate cortex, then cover the work that has demonstrated the overrepresentation of the central region of vision in humans. The common patterns of visual field disturbance caused by damage to the retrochiasmal visual system are discussed, with some less common examples shown as brief case studies.

Hippocampal activity represents many behaviorally important variables, including context, an animal’s location within a given environmental context, time, and reward. Using longitudinal calcium imaging in mice, multiple large virtual environments, and differing reward contingencies, we derived a unified probabilistic model of CA1 representations centered on a single feature—the field propensity. Each cell’s propensity governs how many place fields it has per unit space, predicts its reward-related activity, and is preserved across distinct environments and over months. Propensity is broadly distributed—with many low, and some very high, propensity cells—and thus strongly shapes hippocampal representations. This results in a range of spatial codes, from sparse to dense. Propensity varied ∼10-fold between adjacent cells in salt-and-pepper fashion, indicating substantial functional differences within a presumed cell type. Intracellular recordings linked propensity to cell excitability. The stability of each cell’s propensity across conditions suggests this fundamental property has anatomical, transcriptional, and/or developmental origins.

The avian Wulst is the pallial (analogous to mammalian cortex) termination point of the thalamofugal pathway, one of two main visual pathways in birds, and is considered to be equivalent to primate striate cortex. We recorded neuronal activity from the Wulst in pigeons during two versions of a delayed matching-to-sample procedure. Two birds were trained on a common outcomes (CO) procedure, in which correct responses following both the skateboarder and the flower stimuli were associated with reward. Two other birds were trained on a differential outcomes (DO) procedure in which correct responses following only the skateboarder stimulus were associated with reward, while correct responses following the flower stimulus were not rewarded. In line with previous studies, under CO conditions, and for both excitatory and inhibitory neurons, delay activity in the Wulst was significantly different from baseline activity following both sample stimuli, which may indicate that Wulst delay activity is a neural correlate of working memory for the sample stimulus. On the other hand, under DO conditions, Wulst delay activity appeared to be a neural correlate of the upcoming reward. We argue that Wulst neurons display flexibility in their encoding in that they can encode both sample and reward information, but may default to one type of coding over the other based on the demands of the task. The current study provides the first evidence that delay activity in the Wulst represents both a neural correlate for sample information as well as reward information.

The present review describes recent developments regarding the role of the eye movement system in representing spatial information and keeping track of locations of relevant objects. First, we discuss the active vision perspective and why eye movements are considered crucial for perception and attention. The second part focuses on the question of how the oculomotor system is used to represent spatial attentional priority, and the role of the oculomotor system in maintenance of this spatial information. Lastly, we discuss recent findings demonstrating rapid updating of information across saccadic eye movements. We argue that the eye movement system plays a key role in maintaining and rapidly updating spatial information. Furthermore, we suggest that rapid updating emerges primarily to make sure actions are minimally affected by intervening eye movements, allowing us to efficiently interact with the world around us.

In vivo calcium (Ca²⁺) imaging using two-photon microscopy allows activity to be monitored simultaneously from hundreds of individual neurons within a local population. While this allows us to gain important insights into how cortical neurons represent sensory information, factors such as photo-bleaching of the Ca²⁺ indicator limit imaging duration (and thus the numbers of stimuli that can be tested), which in turn hampers the full characterization of neuronal response properties. Here, we demonstrate that using an encoding model combined with presentation of natural movies results in detailed characterization of receptive field (RF) properties despite the relatively short time for data collection. During presentation of natural movie clips to macaque monkeys, we recorded fluorescence signals from primary visual cortex (V1) neurons that had been loaded with a Ca²⁺ indicator. For each recorded neuron, we constructed an encoding model that comprised an array of motion-energy filters that tiled over the RFs. We optimized the weight of each filter's output so that the linear sum of the outputs across the filters mimicked the neuron's Ca²⁺-signal responses. These models were able to predict the neural responses to a different set of natural movies with a significant degree of accuracy. Moreover, the orientation tunings of neurons simulated by the model were highly correlated with those experimentally obtained when grating stimuli were presented to the monkeys. The model predictions were also consistent with what is known about spatial frequency tunings, the structure of excitatory subfields of RFs (i.e., classical RFs), and functional maps for these RF properties in V1. Further analysis revealed a new aspect of V1 functional architecture; the extent and distribution of suppressive RF subfields varied among nearby neurons, while those for excitatory subfields were shared. Thus, applying our encoding-model analysis to two-photon Ca²⁺ imaging of neuronal responses to natural movies provides a reliable and efficient means of analyzing a wide range of RF properties in multiple neurons imaged in a local region.