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.
cortex; LGN; monkey; oscillations; V1; vision
The circuitry responsible for generating orientation-specific responses in primary visual cortex remains controversial. A new study identifies an anatomical substrate for orientation selectivity and suggests the mechanism may be conserved across species.
Compared to the developing visual system, where neuronal plasticity has been well characterized at multiple levels, little is known about plasticity in the adult, particularly within subcortical structures. We made intraocular injections of 2-amino-4-phosphonobutyric acid (APB) in adult cats to block visual responses in On-center retinal ganglion cells and examined the consequences on visual responses in the lateral geniculate nucleus (LGN) of the thalamus. In contrast to current views of retinogeniculate organization, which hold that On-center LGN neurons should become silent with APB, we find that ~50% of On-center neurons rapidly develop Off-center responses. The time course of these emergent responses and the actions of APB in the retina indicate the plasticity occurs within the LGN. These results suggest there is greater divergence of retinogeniculate connections than previously recognized and that functionally silent, non-specific retinal inputs can serve as a substrate for rapid plasticity in the adult.
thalamus; activity; LGN; retina; APB
Attention is a critical component of perception. However, the mechanisms by which attention modulates neuronal communication to guide behavior 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 (1) increasing the efficacy of presynaptic input in driving postsynaptic responses, (2) increasing synchronous responses among ensembles of postsynaptic neurons receiving independent input, and (3) decreasing redundant signals between postsynaptic neurons receiving common input. These 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 milieu.
This review considers the influential notion of a canonical (cortical) microcircuit in light of recent theories about neuronal processing. Specifically, we conciliate quantitative studies of microcircuitry and the functional logic of neuronal computations. We revisit the established idea that message passing among hierarchical cortical areas implements a form of Bayesian inference – paying careful attention to the implications for intrinsic connections among neuronal populations. By deriving canonical forms for these computations, one can associate specific neuronal populations with specific computational roles. This analysis discloses a remarkable correspondence between the microcircuitry of the cortical column and the connectivity implied by predictive coding. Furthermore, it provides some intuitive insights into the functional asymmetries between feedforward and feedback connections and the characteristic frequencies over which they operate.
neuronal; connectivity; cortical; microcircuit; computation; predictive coding; free energy principle; gamma oscillations; beta oscillations
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.
V1; LGN; primate; temporal; corticogeniculate; vision
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 corticothalamic projection cannot be viewed in isolation, but must be considered as an integral part of a thalamo-cortico-thalamic circuit which intimately interconnects the thalamus and cortex for sensory processing.
The ferret has become a model animal for studies exploring the development of the visual system. However, little is known about the receptive-field structure and response properties of neurons in the adult visual cortex of the ferret. We performed single-unit recordings from neurons in layer 4 of adult ferret primary visual cortex to determine the receptive-field structure and visual-response properties of individual neurons. In particular, we asked what is the spatiotemporal structure of receptive fields of layer 4 neurons and what is the orientation selectivity of layer 4 neurons? Receptive fields of layer 4 neurons were mapped using a white-noise stimulus; orientation selectivity was determined using drifting, sine-wave gratings. Our results show that most neurons (84%) within layer 4 are simple cells with elongated, spatially segregated, ON and OFF subregions. These neurons are also selective for stimulus orientation; peaks in orientation-tuning curves have, on average, a half-width at half-maximum response of 21.5 ± 1.2° (mean ± SD). The remaining neurons in layer 4 (16%) lack orientation selectivity and have center/surround receptive fields. Although the organization of geniculate inputs to layer 4 differs substantially between ferret and cat, our results demonstrate that, like in the cat, most neurons in ferret layer 4 are orientation-selective simple cells.
In addition to the classical, center/surround receptive field of neurons in the lateral geniculate nucleus (LGN), there is an extraclassical, non-linear 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 monkey 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 surround suppression in the macaque LGN relies on feedforward mechanisms and suggest that suppression in the cortex likely includes a component established in the retina.
V1; LGN; feedback; corticogeniculate; receptive field
Periodic activity patterns or oscillations within the gamma frequency band (20–80 Hz) have been implicated in sensory processing and cognition in many areas of the cerebral cortex, including primary visual cortex (V1). Although periodic activity appears to be a hallmark of cortical neurons, little is known about the dynamics of these activity patterns as signals progress within local cortical circuits. This study compares the strength of periodic activity between neurons in the input and output stages of cortical processing – neurons in layers 4 and 6 – of V1 in the alert macaque monkey. Our results demonstrate that while both populations of neurons display significant gamma-band activity, this activity increases from the input to output layers of the cortex. These data suggest that local cortical circuits enhance periodic activity within a cortical area.
V1; LGN; geniculocortical; corticogeniculate
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.
LGN; V1; corticogeniculate; geniculocortical
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.
V1; LGN; lateral geniculate nucleus; spike rate; coding
Most neurons in primary visual cortex (V1) are selective for stimulus size, a property with important implications for salient feature detection. Size selectivity involves dynamic interactions between neuronal circuits that establish the classical (center) and extraclassical (surround) of a neuron’s receptive field. Although much is known about the tuning properties and stimulus selectivity of the center and surround subunits, relatively little is known about how these subunits interact to achieve size selectivity. In order to address this question, we examined the temporal dynamics of size selectivity in two classes of pyramidal neurons at similar hierarchical processing stages in V1 of alert monkeys. These two classes were comprised of neurons in cortical layer 6 with identified projections to the lateral geniculate nucleus. While both neuronal groups displayed comparable levels of size selectivity, the temporal dynamics of their tuning differed significantly. We compared the size tuning profiles of each cell type with a series of sum-of-Gaussian models and discovered that the receptive fields of neurons with fast-conducting axons contained an excitatory center and a suppressive surround with similar onset timing. In contrast, neurons with slow-conducting axons utilized two center components—an early wide-field component and a delayed narrow-field component that increased activity—in addition to the surround component. The early, wide-field component represents a novel mechanism for cortical neurons to integrate contextual information. These results demonstrate that size tuning in cortical neurons is established via multiple unique mechanisms, dictated by the rich circuit architecture in which neurons are embedded.
receptive field; surround suppression; spatial; temporal; V1; corticogeniculate
Spatial selective attention is the mechanism that facilitates the selection of relevant information over irrelevant information in the visual field. The current study investigated whether foreknowledge of the presence or absence of distractors surrounding an impending target stimulus results in preparatory changes in visual cortex. We cued the location of the target and the presence or absence of distractors surrounding the target while changes in blood oxygen level dependent (BOLD) signals were measured. In line with prior work, we found that top-down spatial attention resulted in an increased contralateral BOLD response, evoked by the cue throughout early visual cortex (areas V1, V2 and V3). In addition, cues indicating distractor presence evoked a substantial increase in the magnitude of the BOLD signal in visual area V3, but not in V2 or V1. This study shows that prior knowledge concerning the presence of a distractor results in enhanced attentional modulation of visual cortex, in visual areas where neuronal receptive fields are large enough to encompass both targets and distractors. We interpret these findings as evidence that top-down attentional control processes include active preparatory suppression mechanisms for irrelevant, distracting information in the visual scene.
This study examines the rules governing the transfer of spikes between the retina and LGN with the goal of determining whether the most informative retinal spikes preferentially drive LGN responses and what role spike timing plays in the process. By recording from monosynaptically-connected pairs of retinal ganglion cells and LGN neurons in vivo in the cat, we show that relayed spikes are more likely than non-relayed spikes to be evoked by stimuli that match the recorded cells’ receptive fields and that an interspike interval (ISI)-based mechanism contributes to the process. Relayed spikes are also more reliable in their timing and number where they often achieve the theoretical limit of minimum variance. As a result, relayed spikes carry more visual information per spike. Based on these results, we conclude that retinogeniculate processing increases sparseness in the neural code by selectively relaying the highest fidelity spikes to the visual cortex.
coding; retina; LGN; retinal ganglion cell; receptive field; cat
Although corticothalamic feedback is ubiquitous across species and modalities, its role in sensory processing is unclear. This study provides the first 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.
feedback; corticothalamic; V1; LGN; thalamus
The cerebral cortex is a vastly complex structure consisting of multiple distinct populations of neurons residing in functionally specialized cortical compartments. A fundamental goal in systems neuroscience is to understand the interactions among cortical neurons and their relationship to behavior. It is hypothesized that dynamic activity patterns, such as oscillations in global neuronal activity, could span large, heterogeneous populations of cortical neurons in such a manner as to bind together the activity of otherwise disparate cortical networks. Little is known about the mechanisms by which such global oscillatory patterns entrain cortical networks, or the contribution of such activity patterns to cortical function. An important step toward elucidating the role of such patterned activity in cortical information processing is understanding these interactions at the local circuit level. Here, we highlight recent findings that provide insight into how dynamic activity patterns affect specific neuronal populations and circuits.
gamma-band; oscillation; cortical circuit; geniculocortical; corticogeniculate
The interspike interval (ISI) preceding a retinal spike has a strong influence on whether retinal spikes will drive postsynaptic responses in the lateral geniculate nucleus (LGN). This ISI-based filtering of retinal spikes could, in principle, be used as a mechanism for processing visual information en route from retina to cortex; however, this form of processing has not been previously explored. Using a white noise stimulus and reverse correlation analysis, we compared the receptive fields associated with retinal spikes over a range of ISIs (0–120 ms). Results showed that, although the location and sign of retinal ganglion cell receptive fields are invariant to ISI, the size and amplitude of receptive fields vary with ISI. These results support the notion that ISI-based filtering of retinal spikes can serve as a mechanism for shaping receptive fields.
Thalamic relay cells fire action potentials that transmit information from retina to cortex. The amount of information that spike trains encode is usually estimated from the precision of spike timing with respect to the stimulus. Sensory input, however, is only one factor that influences neural activity. For example, intrinsic dynamics, such as oscillations of networks of neurons, also modulate firing pattern. Here, we asked if retinal oscillations might help to convey information to neurons downstream. Specifically, we made whole-cell recordings from relay cells to reveal retinal inputs (EPSPs) and thalamic outputs (spikes) and then analyzed these events with information theory. Our results show that thalamic spike trains operate as two multiplexed channels. One channel, which occupies a low frequency band (<30 Hz), is encoded by average firing rate with respect to the stimulus and carries information about local changes in the visual field over time. The other operates in the gamma frequency band (40–80 Hz) and is encoded by spike timing relative to retinal oscillations. At times, the second channel conveyed even more information than the first. Because retinal oscillations involve extensive networks of ganglion cells, it is likely that the second channel transmits information about global features of the visual scene.
LGN; retina; visual coding; natural stimuli; oscillations
Although the visual response properties of neurons along the retinogeniculocortical pathway have been studied for decades, relatively few studies have examined how individual neurons along the pathway communicate with each other. Recent studies in the cat (Felis domestica) now show that the strength of these connections is very dynamic and spike timing plays an important part in determining whether action potentials will be transferred from pre- to postsynaptic cells. This review explores recent progress in our understanding of what role spike timing has in establishing different patterns of geniculate activity and how these patterns ultimately drive the cortex.