Henry J. Alitto

Corticothalamic feedback and sensory processing.

Although nearly half of the synaptic input to neurons in the dorsal thalamus comes from the cerebral cortex, the role of corticothalamic projections in sensory processing remains elusive. Although sensory afferents certainly establish the basic receptive field properties of thalamic neurons, increasing evidence indicates that feedback from the cortex plays a crucial role in shaping thalamic responses. Here, we review recent work on the corticothalamic pathways associated with the visual, auditory, and somatosensory systems. Collectively, these studies demonstrate that sensory responses of thalamic neurons result from dynamic interactions between feedforward and feedback pathways.

Origin and Dynamics of Extraclassical Suppression in the Lateral Geniculate Nucleus of the Macaque Monkey

In addition to the classical, center/surround receptive field of neurons in the lateral geniculate nucleus (LGN), there is an extraclassical, nonlinear surround that can strongly suppress LGN responses. This form of suppression likely plays an important role in adjusting the gain of LGN responses to visual stimuli. We performed experiments in alert and anesthetized macaque monkies to quantify extraclassical suppression in the LGN and determine the roles of feedforward and feedback pathways in the generation of LGN suppression. Results show that suppression is significantly stronger among magnocellular neurons than parvocellular neurons and that suppression arises too quickly for involvement from cortical feedback. Furthermore, the amount of suppression supplied by the retina is not significantly different from that in the LGN. These results indicate that extraclassical suppression in the macaque LGN relies on feedforward mechanisms and suggest that suppression in the cortex likely includes a component established in the retina.

Distinct Properties of Stimulus-Evoked Bursts in the Lateral Geniculate Nucleus

Neurons in the lateral geniculate nucleus (LGN) of the thalamus produce spikes that can be classified as burst spikes and tonic spikes. Although burst spikes are generally associated with states of sleep and drowsiness, bursts may also play an important role in sensory processing. This study explores the stimulus properties that evoke burst and tonic spikes and examines the reliability of LGN neurons to produce visually driven bursts. Using reverse-correlation techniques, we show that the receptive fields of burst spikes are similar to, but significantly different from, the receptive fields of tonic spikes. Compared with tonic spikes, burst spikes (1) occur with a shorter latency between stimulus and response, (2) have a greater dependence on stimuli with transitions from suppressive to preferred states, and (3) prefer stimuli that provide increased drive to the receptive field center and even greater increased drive to the receptive field surround. These differences are not attributable to the long interspike interval that precedes burst spikes, because tonic spikes with similar preceding interspike intervals also differ from burst spikes in both the spatial and temporal domains. Finally, measures of reliability are significantly greater for burst spikes than for tonic spikes with similar preceding interspike intervals. These results demonstrate that thalamic bursts contribute to sensory processing and can reliably provide the cortex with information that is similar to, but distinct from, that of tonic spikes.

A comparison of visual responses in the lateral geniculate nucleus of alert and anaesthetized macaque monkeys

Neurons in the lateral geniculate nucleus (LGN) of the thalamus are the major source of visual input to the cerebral cortex. Much of our understanding of the physiology of LGN neurons comes from data collected in anaesthetized animals. This study examines the visual responses of LGN neurons in alert animals and compares these responses to those from anaesthetized animals. Compared to the anaesthetized animal, LGN neurons in the alert animal respond to visual stimuli with stronger responses and follow stimuli drifting at higher spatial and temporal frequencies. Stronger responses are likely to translate into an increased coupling between the LGN and visual cortex, as firing rate and interspike interval are known to influence the dynamics of synaptic communication between the two structures.

Visual Functions of the Thalamus

The thalamus is the heavily interconnected partner of the neocortex. All areas of the neocortex receive afferent input from and send efferent projections to specific thalamic nuclei. Through these connections, the thalamus serves to provide the cortex with sensory input, and to facilitate interareal cortical communication and motor and cognitive functions. In the visual system, the lateral geniculate nucleus (LGN) of the dorsal thalamus is the gateway through which visual information reaches the cerebral cortex. Visual processing in the LGN includes spatial and temporal influences on visual signals that serve to adjust response gain, transform the temporal structure of retinal activity patterns, and increase the signal-to-noise ratio of the retinal signal while preserving its basic content. This review examines recent advances in our understanding of LGN function and circuit organization and places these findings in a historical context.

Dynamic properties of thalamic neurons for vision.

A striking property of neurons in the lateral geniculate nucleus (LGN) of the thalamus is the ability to dynamically filter and transform the temporal structure of their retinal spike input. In particular, LGN neurons respond to visual stimuli with either burst spike responses or tonic spike responses. While much is known from in vitro studies about the cellular mechanisms that underlie burst and tonic spikes, relatively little is known about the sensory stimuli that evoke these two categories of spikes. This review examines recent progress that has been made towards understanding the spatiotemporal properties of visual stimuli that evoke burst and tonic spikes. Using white-noise stimuli and reverse-correlation analysis, results show that burst and tonic spikes carry similar, but distinct, information to cortex. Compared to tonic spikes, burst spikes (1) occur with a shorter latency between stimulus and response, (2) have a greater dependence on stimuli with transitions from suppressive to preferred states, and (3) prefer stimuli that provide increased drive to the receptive field center and even greater increased drive to the receptive field surround. These results are discussed with an emphasis placed on relating the cellular constraints for burst and tonic activity with the functional properties of the early visual pathway during sensory processing.

Stimulus Contrast and Retinogeniculate Signal Processing.

Neuronal signals conveying luminance contrast play a key role in nearly all aspects of perception, including depth perception, texture discrimination, and motion perception. Although much is known about the retinal mechanisms responsible for encoding contrast information, relatively little is known about the relationship between stimulus contrast and the processing of neuronal signals between visual structures. Here, we describe simultaneous recordings from monosynaptically connected retinal ganglion cells and lateral geniculate nucleus (LGN) neurons in the cat to determine how stimulus contrast affects the communication of visual signals between the two structures. Our results indicate that: (1) LGN neurons typically reach their half-maximal response at lower contrasts than their individual retinal inputs and (2) LGN neurons exhibit greater contrast-dependent phase advance (CDPA) than their retinal inputs. Further analyses suggests that increased sensitivity relies on spatial convergence of multiple retinal inputs, while increased CDPA is achieved, in part, on temporal summation of arriving signals.

Surround suppression and temporal processing of visual signals

Extraclassical surround suppression strongly modulates responses of neurons in the retina, lateral geniculate nucleus (LGN), and primary visual cortex. Although a great deal is known about the spatial properties of extraclassical suppression and the role it serves in stimulus size tuning, relatively little is known about how extraclassical suppression shapes visual processing in the temporal domain. We recorded the spiking activity of retinal ganglion cells and LGN neurons in the cat to test the hypothesis that extraclassical suppression influences temporal features of visual responses in the early visual system. Our results demonstrate that extraclassical suppression not only shifts the distribution of interspike intervals in a manner that decreases the efficacy of neuronal communication, it also decreases the reliability of neuronal responses to visual stimuli and it decreases the duration of visual responses, an effect that underlies a rightward shift in the temporal frequency tuning of LGN neurons. Taken together, these results reveal a dynamic relationship between extraclassical suppression and the temporal features of neuronal responses.

Dissecting the Dynamics of Corticothalamic Feedback

The thalamus and neocortex are intimately interconnected via a reciprocal arrangement of feedforward and feedback projections. In this issue of Neuron, Crandall et al. (2015) provide key insight into the functional dynamics of feedback projections and reveal the cellular and circuit mechanisms that underlie a rate-dependent switch in the net influence, suppression versus excitation, that cortex can exert on thalamic relay cells.

The augmentation of retinogeniculate communication during thalamic burst mode

Retinal signals are transmitted to cortex via neurons in the lateral geniculate nucleus (LGN), where they are processed in burst or tonic response mode. Burst mode occurs when LGN neurons are sufficiently hyperpolarized for T-Type Ca2+ channels to de-inactivate, allowing them to open in response to a depolarization which can trigger a high-frequency sequence of Na+-based spikes (i.e. burst). In contrast, T-type channels are inactivated during tonic mode and do not contribute to spiking. Although burst mode is commonly associated with sleep and the disruption of retinogeniculate communication, bursts can also be triggered by visual stimulation, thereby transforming the retinal signals relayed to the cortex. To determine how burst mode affects retinogeniculate communication, we made recordings from monosynaptically connected retinal ganglion cells and LGN neurons in the cat during visual stimulation. Our results reveal a robust augmentation of retinal signals within the LGN during burst mode. Specifically, retinal spikes were more effective and often triggered multiple LGN spikes during periods likely to have increased T-Type Ca2+ activity. Consistent with the biophysical properties of T-Type Ca2+ channels, analysis revealed that effect magnitude was correlated with the duration of the preceding thalamic interspike interval and occurred even in the absence of classically defined bursts. Importantly, the augmentation of geniculate responses to retinal input was not associated with a degradation of visual signals. Together, these results indicate a graded nature of response mode and suggest that, under certain conditions, bursts facilitate the transmission of visual information to the cortex by amplifying retinal signals. Significance The thalamus is the gateway for retinal information traveling to the cortex. The lateral geniculate nucleus (LGN), like all thalamic nuclei, has two classically defined categories of spikes—tonic and burst—that differ in their underlying cellular mechanisms. Here we compare retinogeniculate communication during burst and tonic response modes. Our results show that retinogeniculate communication is enhanced during burst mode and visually evoked thalamic bursts, thereby augmenting retinal signals transmitted to cortex. Further, our results demonstrate that the influence of burst mode on retinogeniculate communication is graded and can be measured even in the absence of classically defined thalamic bursts.