Matthew W. Self

The lateral geniculate nucleus (LGN) of the thalamus is a key link between the retina and visual cortex but our understanding of the properties of neurons in the human LGN is based on recordings in animal models. Here we recorded spiking activity of cells in the LGN of two patients who had electrodes implanted in the LGN as part of their treatment for epilepsy. Human LGN cells responded to strong visual stimulation with high-frequency bursts of spikes. The cells had receptive-field properties resembling those of monkeys with circular ON-OFF sub-fields, red-green opponency in the dorsal layers and preferences for high temporal frequencies in the ventral layers. Responses were largely monocular and the closure of one eye decreased the spontaneous activity of broad-spiking neurons preferring this eye while increasing the activity of neurons with narrower spikes, suggesting that interneurons might gate LGN activity during eye closure.

Our perception of contrast is strongly affected by contextual factors. A well-known example is that of orientation-tuned surround suppression (OTSS). Surrounds have more suppressive effects on the perceived contrast of the center when they have the same orientation. This phenomenon has been linked to horizontal interactions within the early visual cortex. Here we show that the strength of suppression is modulated strongly by the perceived three-dimensional structure of the scene. Placing the surround at a different retinal disparity, and therefore perceived depth, decreased OTSS, regardless of whether the surround was placed behind or in front of the center. The difference in disparity was, however, not the key determinant of the strength of OTSS. Suppressive interactions were strongest when the surround formed a three-dimensional surface that was continuous with the center and weaker when the surround seemed to be part of a separate surface, even when the surround seemed to be closer to the center in perceived depth. The results suggest that visual features that are perceived to form part of the same surface can engage in stronger suppressive interactions than those perceived to lie on different surfaces. This raises questions about how the underlying neural interactions become restricted to surfaces and support the view that top-down information about perceptual organization can gate interactions occurring at lower levels in the visual system.

We recorded spiking activity in the human lateral geniculate nucleus (LGN), which links the retina with the primary visual cortex. The cells had receptive-field properties resembling those of monkeys. Responses were largely monocular and the closure of one eye decreased the spontaneous activity of neurons with broader spikes preferring this eye and increased the activity of neurons with narrower spikes, suggesting that interneurons might gate LGN activity during eye closure.

The visual system needs to identify perceptually relevant borders to segment complex natural scenes. The primary visual cortex (V1) is thought to extract local borders, and higher visual areas are thought to identify the perceptually relevant borders between objects and the background. To test this conjecture, we used natural images that had been annotated by human observers who marked the perceptually relevant borders. We assessed the effect of perceptual relevance on V1 responses using human neuroimaging, macaque electrophysiology, and computational modeling. We report that perceptually relevant borders elicit stronger responses in the early visual cortex than irrelevant ones, even if simple features, such as contrast and the energy of oriented filters, are matched. Moreover, V1 neurons discriminate perceptually relevant borders surprisingly fast, during the early feedforward-driven activity at a latency of ~50 ms, indicating that they are tuned to the features that characterize them. We also revealed a delayed, contextual effect that enhances the V1 responses that are elicited by perceptually relevant borders at a longer latency. Our results reveal multiple mechanisms that allow V1 neurons to infer the layout of objects in natural images.

Cortical feedback connections are extremely numerous but the logic of connectivity between higher and lower areas remains poorly understood. Feedback from higher visual areas to primary visual cortex (V1) has been shown to enhance responses on perceptual figures compared to backgrounds, an effect known as figure-background modulation (FBM). A likely source of this feedback are border-ownership (BO) selective cells in mid-tier visual areas (e.g. V4) which represent the location of figures. We examined the connectivity between V4 cells and V1 cells using noise-correlations and micro-stimulation to estimate connectivity strength. We show that connectivity is consistent with a model in which BO-tuned V4 cells send positive feedback in the direction of their preferred figure and negative feedback in the opposite direction. This connectivity scheme can recreate patterns of FBM observed in previous studies. These results provide insights into the cortical connectivity underlying figure-background perception and establish a link between FBM and BO-tuning.

During discourse comprehension, every new word adds to an evolving representation of meaning that accumulates over consecutive sentences and constrains the next words. To minimize repetition and utterance length, languages use pronouns, like the word “she,” to refer to nouns and phrases that were previously introduced. It has been suggested that language comprehension requires that pronouns activate the same neuronal representations as the nouns themselves. We recorded from individual neurons in the human hippocampus during a reading task. Cells that were selective to a particular noun were later reactivated by pronouns that refer to the cells’ preferred noun. These results imply that concept cells contribute to a rapid and dynamic semantic memory network that is recruited during language comprehension.

Detailed characterization of interneuron types in primary visual cortex (V1) has greatly contributed to understanding visual perception, yet the role of chandelier cells (ChCs) in visual processing remains poorly characterized. Using viral tracing we found that V1 ChCs predominantly receive monosynaptic input from local layer 5 pyramidal cells and higher-order cortical regions. Two-photon calcium imaging and convolutional neural network modeling revealed that ChCs are visually responsive but weakly selective for stimulus content. In mice running in a virtual tunnel, ChCs respond strongly to events known to elicit arousal, including locomotion and visuomotor mismatch. Repeated exposure of the mice to the virtual tunnel was accompanied by reduced visual responses of ChCs and structural plasticity of ChC boutons and axon initial segment length. Finally, ChCs only weakly inhibited pyramidal cells. These findings suggest that ChCs provide an arousal-related signal to layer 2/3 pyramidal cells that may modulate their activity and/or gate plasticity of their axon initial segments during behaviorally relevant events.

Neurons in the primary visual cortex (V1) respond to stimuli in their receptive field (RF), which is defined by the feedforward input from the retina. However, V1 neurons are also sensitive to contextual information outside their RF, even if the RF itself is unstimulated. Here, we examined the cortical circuits for V1 contextual responses to gray disks superimposed on different backgrounds. Contextual responses began late and were strongest in the feedback-recipient layers of V1. They differed between the three main classes of inhibitory neurons, with particularly strong contextual drive of VIP neurons, indicating a contribution of disinhibitory circuits to contextual drive. Contextual drive was strongest when the gray disk was perceived as figure, occluding its background, rather than a hole. Our results link contextual drive in V1 to perceptual organization and provide previously unknown insight into how recurrent processing shapes the response of sensory neurons to facilitate figure perception.

Theta and gamma oscillations in the medial temporal lobe are suggested to play a critical role for human memory formation via establishing synchrony in neural assemblies. Arguably, such synchrony facilitates efficient information transfer between neurons and enhances synaptic plasticity, both of which benefit episodic memory formation. However, to date little evidence exists from humans that would provide direct evidence for such a specific role of theta and gamma oscillations for episodic memory formation. Here, we investigate how oscillations shape the temporal structure of neural firing during memory formation in the medial temporal lobe. We measured neural firing and local field potentials in human epilepsy patients via micro-wire electrode recordings to analyze whether brain oscillations are related to co-incidences of firing between neurons during successful and unsuccessful encoding of episodic memories. The results show that phase-coupling of neurons to faster theta and gamma oscillations correlates with co-firing at short latencies (~20–30 ms) and occurs during successful memory formation. Phase-coupling at slower oscillations in these same frequency bands, in contrast, correlates with longer co-firing latencies and occurs during memory failure. Thus, our findings suggest that neural oscillations play a role for the synchronization of neural firing in the medial temporal lobe during the encoding of episodic memories.

Neuronal activity in the primary visual cortex (V1) is driven by feedforward input from within the neurons’ receptive fields (RFs) and modulated by contextual information in regions surrounding the RF. The effect of contextual information on spiking activity occurs rapidly, and is therefore challenging to dissociate from feedforward input. To address this challenge, we recorded the spiking activity of V1 neurons in monkeys viewing either natural scenes or scenes where the information in the RF was occluded, effectively removing the feedforward input. We found that V1 neurons responded rapidly and selectively to occluded scenes. V1 responses elicited by occluded stimuli could be used to decode scene identity and could be predicted from those elicited by non-occluded images, indicating that there is overlap between visually-driven and contextual responses. We used representational similarity analysis to show that the structure of V1 representations of occluded scenes measured with electrophysiology in monkeys correlates strongly with the representations of the same scenes in humans measured with fMRI. Our results reveal that contextual influences alter the spiking activity of V1 in monkeys across large distances on a rapid time scale, carry information about scene identity and resemble those in human V1.