Farran Briggs

Emerging views of corticothalamic function.

Although it is now generally accepted that the thalamus is more than a simple relay of sensory signals to the cortex, we are just beginning to gain an understanding of how corticothalamic feedback influences sensory processing. Results from an increasing number of studies across sensory systems and different species reveal effects of feedback both on the receptive fields of thalamic neurons and on the transmission of sensory information between the thalamus and cortex. Importantly, these studies demonstrate that the cortico-thalamic projection cannot be viewed in isolation, but must be considered as an integral part of a thalamo-corticothalamic circuit which intimately interconnects the thalamus and cortex for sensory processing.

Attention enhances synaptic efficacy and the signal-to-noise ratio in neural circuits

Attention is a critical component of perception. However, the mechanisms by which attention modulates neuronal communication to guide behaviour are poorly understood. To elucidate the synaptic mechanisms of attention, we developed a sensitive assay of attentional modulation of neuronal communication. In alert monkeys performing a visual spatial attention task, we probed thalamocortical communication by electrically stimulating neurons in the lateral geniculate nucleus of the thalamus while simultaneously recording shock-evoked responses from monosynaptically connected neurons in primary visual cortex. We found that attention enhances neuronal communication by increasing the efficacy of presynaptic input in driving postsynaptic responses, by increasing synchronous responses among ensembles of postsynaptic neurons receiving independent input, and by decreasing redundant signals between postsynaptic neurons receiving common input. The results demonstrate that attention finely tunes neuronal communication at the synaptic level by selectively altering synaptic weights, enabling enhanced detection of salient events in the noisy sensory environment.

Organizing principles of cortical layer 6

Neurons in the deepest layer of mammalian cerebral cortex are morphologically and physiological diverse and are situated in a strategic position to modulate neuronal activity locally and in other structures. The variety of neuronal circuits within which layer 6 neurons participate differs across species and cortical regions. However even amidst this diversity, common organizational features emerge. Examination of the anatomical and physiological characteristics of different classes of layer 6 neuron, each specialized to participate in distinct circuits, provides insight into the functional contributions of layer 6 neurons toward cortical information processing.

Parallel Processing in the Corticogeniculate Pathway of the Macaque Monkey

Although corticothalamic feedback is ubiquitous across species and modalities, its role in sensory processing is unclear. This study provides a detailed description of the visual physiology of corticogeniculate neurons in the primate. Using electrical stimulation to identify corticogeniculate neurons, we distinguish three groups of neurons with response properties that closely resemble those of neurons in the magnocellular, parvocellular, and koniocellular layers of their target structure, the lateral geniculate nucleus (LGN) of the thalamus. Our results indicate that corticogeniculate feedback in the primate is stream specific, and provide strong evidence in support of the view that corticothalamic feedback can influence the transmission of sensory information from the thalamus to the cortex in a stream-selective manner.

A Fast, Reciprocal Pathway between the Lateral Geniculate Nucleus and Visual Cortex in the Macaque Monkey

Neurons in the lateral geniculate nucleus (LGN) not only provide feedforward input to primary visual cortex (V1), but also receive robust feedback from the cortex. Accordingly, visual processing in the LGN is continuously influenced by previous patterns of activity. This study examines the temporal properties of feedforward and feedback pathways between the LGN and V1 in the macaque monkey to provide a lower bound on how quickly the cortex can influence the LGN. In so doing, we identified a subclass of corticogeniculate neurons that receives direct, suprathreshold input from the LGN that is similar in latency to that directed to other recipient neurons (4.2 ± 0.4 vs 4.0 ± 0.2 ms). These neurons also provide feedback to the LGN that is significantly shorter in latency than that supplied by corticogeniculate neurons lacking LGN input (5.1 ± 1.3 vs 11.1 ± 2.3 ms, respectively). Across our sample of corticogeniculate neurons, the shortest combined visual response latency and feedback latency was 37 ms (mean, 52.5 ± 3.8 ms), indicating that visual signals can rapidly travel from the periphery to the cortex and back to the LGN.

Corticogeniculate feedback and visual processing in the primate.

Corticogeniculate neurones make more synapses in the lateral geniculate nucleus (LGN) than retinal ganglion cells, yet we know relatively little about the functions of corticogeniculate feedback for visual processing. In primates, feedforward projections from the retina to the LGN and from the LGN to primary visual cortex are organized into anatomically and physiologically distinct parallel pathways. Recent work demonstrates a close relationship between these parallel streams of feedforward projections and the corticogeniculate feedback pathway. Here, we review the evidence for stream‐specific feedback in the primate and consider the implications of parallel streams of feedback for vision.

Simultaneous Recordings from the Primary Visual Cortex and Lateral Geniculate Nucleus Reveal Rhythmic Interactions and a Cortical Source for Gamma-Band Oscillations

Oscillatory synchronization of neuronal activity has been proposed as a mechanism to modulate effective connectivity between interacting neuronal populations. In the visual system, oscillations in the gamma-frequency range (30–100 Hz) are thought to subserve corticocortical communication. To test whether a similar mechanism might influence subcortical-cortical communication, we recorded local field potential activity from retinotopically aligned regions in the lateral geniculate nucleus (LGN) and primary visual cortex (V1) of alert macaque monkeys viewing stimuli known to produce strong cortical gamma-band oscillations. As predicted, we found robust gamma-band power in V1. In contrast, visual stimulation did not evoke gamma-band activity in the LGN. Interestingly, an analysis of oscillatory phase synchronization of LGN and V1 activity identified synchronization in the alpha (8–14 Hz) and beta (15–30 Hz) frequency bands. Further analysis of directed connectivity revealed that alpha-band interactions mediated corticogeniculate feedback processing, whereas beta-band interactions mediated geniculocortical feedforward processing. These results demonstrate that although the LGN and V1 display functional interactions in the lower frequency bands, gamma-band activity in the alert monkey is largely an emergent property of cortex.

Morphological Substrates for Parallel Streams of Corticogeniculate Feedback Originating in Both V1 and V2 of the Macaque Monkey

Corticothalamic circuits are essential for reciprocal information exchange between the thalamus and cerebral cortex. Nevertheless, the role of corticothalamic circuits in sensory processing remains a mystery. In the visual system, afferents from retina to the lateral geniculate nucleus (LGN) and from LGN to primary visual cortex (V1) are organized into functionally distinct parallel processing streams. Physiological evidence suggests corticogeniculate feedback may be organized into parallel streams; however, little is known about the diversity of corticogeniculate neurons, their local computations, or the structure-function relationship among corticogeniculate neurons. We used a virus-mediated approach to label and reconstruct the complete dendritic and local axonal arbors of identified corticogeniculate neurons in the macaque monkey. Our results reveal morphological substrates for parallel streams of corticogeniculate feedback based on distinct classes of neurons in V1 and V2. These results support the hypothesis that distinct populations of feedback neurons provide independent and unique information to the LGN.

Temporal properties of feedforward and feedback pathways between the thalamus and visual cortex in the ferret

This study examines the temporal properties of geniculocortical and corticogeniculate (CG) pathways that link the lateral geniculate nucleus (LGN) and primary visual cortex in the ferret. Using electrical stimulation in the LGN to evoke action potentials in geniculocortical and CG axons, results show that conduction latencies are significantly faster in geniculocortical neurons than in CG neurons. Within each pathway, axonal latency and visual physiology support the view of sub-classes of neurons. By examining the timing of visual responses and the latency of CG feedback, estimates indicate that visual information can reach the cortex and return to the LGN as early as 60 msec following the onset of a visual stimulus. These findings place constraints on the functional role of corticogeniculate feedback for visual processing.

Cortical activity influences geniculocortical spike efficacy in the macaque monkey.

Thalamocortical communication is a dynamic process influenced by both presynaptic and postsynaptic mechanisms. In this study, we recorded single-unit responses from cortical neurons that received direct input from the lateral geniculate nucleus (LGN) to address the question of whether prior patterns of cortical activity affect the ability of LGN inputs to drive cortical responses. By examining the ongoing activity that preceded the arrival of electrically evoked spikes from the LGN, we identified a number of activity patterns that were predictive of suprathreshold communication. Namely, cortical neurons were more likely to respond to LGN stimulation when their activity levels increased to 30-40Hz and/or their activity displayed rhythmic patterns (30 ms intervals) with increased power in the gamma frequency band. Cortical neurons were also more likely to respond to LGN stimulation when their activity increased 30-40 ms prior to stimulation, suggesting that the phase of gamma activity also contributes to geniculocortical communication. Based on these results, we conclude that ongoing activity in the cortex is not random, but rather organized in a manner that can influence the dynamics of thalamocortical communication.