Feature-linked synchronization of thalamic relay cell firing induced by feedback from the visual cortex

Nature ◽  
1994 ◽  
Vol 369 (6480) ◽  
pp. 479-482 ◽  
Author(s):  
Adam M. Sillito ◽  
Helen E. Jones ◽  
George L. Gerstein ◽  
David C. West
Author(s):  
Christof Koch

Some neurons throughout the animal kingdom respond to an intracellular current injection or to an appropriate sensory stimulus with a stereotypical sequence of two to five fast spikes riding upon a slow depolarizing envelope. The entire event, termed a burst, is over within 10-40 msec and is usually terminated by a profound afterhyperpolarization (ΑΗΡ). Such bursting cells are not a random feature of a certain fraction of all cells but can be identified with specific neuronal subpopulations. What are the mechanisms generating this intrinsic firing pattern and what is its meaning? Bursting cells can easily be distinguished from a cell firing at a high maintained frequency by the fact that bursts will persist even at a low firing frequency. As illustrated by the thalamic relay cell of Fig. 9.4, some cells can switch between a mode in which they predominantly respond to stimuli via single, isolated spikes and one in which bursts are common. Because we believe that bursting constitutes a special manner of signaling important information, we devote a single, albeit small chapter to this topic. In the following, we describe a unique class of cells that frequently signal with bursts, and we touch upon the possible biophysical mechanisms that give rise to bursting. We finish this excursion by focussing on a functional study of bursting cells in the electric fish and speculate about the functional relevance of burst firing. Neocortical cells are frequently classified according to their response to sustained current injections. While these distinctions are not all or none, there is broad agreement for three classes: regular spiking, fast spiking, and intrinsically bursting neurons (Connors, Gutnick, and Prince, 1982; McCormick et al., 1985; Connors and Gutnick, 1990; Agmon and Connors, 1992; Baranyi, Szente, and Woody, 1993; Nuńez, Amzica, and Steriade, 1993; Gutnick and Crill, 1995; Gray and McCormick, 1996). Additional cell classes have been identified (e.g., the chattering cells that fire bursts of spikes with interburst intervals ranging from 15 to 50 msec; Gray and McCormick, 1996), but whether or not they occur widely has not yet been settled. The cells of interest to us are the intrinsically bursting cells.


2002 ◽  
Vol 16 (4) ◽  
pp. 771-776 ◽  
Author(s):  
Vietminh Paz-Villagràn ◽  
Pierre-Pascal Lenck-Santini ◽  
Etienne Save ◽  
Bruno Poucet
Keyword(s):  

1977 ◽  
Vol 40 (2) ◽  
pp. 410-427 ◽  
Author(s):  
M. W. Dubin ◽  
B. G. Cleland

1. Two groups of interneurons that are involved in the organization of the lateral geniculate nucleus (LGN) are described. The cell bodies of one group lie within the LGN; these units are referred to as intrageniculate. The cell bodies of the other group are found immediately above the LGN at its border with the perigeniculate nucleus; these units are referred to as perigeniculate. 2. Intrageniculate interneurons have center-surround receptive fields that resemble those of relay (principal) cells. They can be subdivided into brisk or sluggish and sustained or transient categories. They are stimulated transsynaptically from the visual cortex and have a characteristic variation in the latency of their spike response to such stimulation both at threshold and for suprathreshold stimuli. The pathway for this stimulation appears to be via cortical efferents to the LGN. Intrageniculate interneurons receive direct, monosynaptic retinal inputs, as determined by recording simultaneously from such interneurons and from the ganglion cells which provide excitatory input to them. Similar to relay cells, they are shown to have one or two major ganglion cell inputs. 3. Perigeniculate interneurons are generally binocularly innervated and give on-off responses to small spot stimuli throughout their receptive field. They respond well to rapid movement of large targets. They respond to electrical stimulation of the retina with a spike latency that falls between that of brisk transient and brisk sustained relay cells. This latency is one synaptic delay longer than that of brisk transient relay cell activation and suggests that they are excited by axon collaterals of these relay cells. Electrical stimulation of the visual cortex is also consistent with this model; the latency of the response of perigeniculate interneurons is approximately one synaptic delay longer than the latency of the response of brisk transient relay cells. 4. The interneuronal pathways described are consistent with proposed circuits that subserve the generation of IPSPs that arise in response to optic nerve and visual cortical stimulation. We now show that such inhibition has feed-forward (intrageniculate) and feed-back (perigeniculate) components that are mediated by two different classes of geniculate interneurons. It is suggested that the intrageniculate interneurons are involved in precise, spatially organized inhibition and that the perigeniculate interneurons are part of a more general, diffuse inhibitory system that modulates LGN excitability.


2016 ◽  
Vol 115 (3) ◽  
pp. 1533-1541 ◽  
Author(s):  
Iman T. Jhangiani-Jashanmal ◽  
Ryo Yamamoto ◽  
Nur Zeynep Gungor ◽  
Denis Paré

The central medial thalamic (CMT) nucleus is a poorly known component of the middle thalamic complex that relays nociceptive inputs to the basolateral amygdala and cingulate cortex and plays a critical role in the control of awareness. The present study was undertaken to characterize the electroresponsive properties of CMT neurons. Similar to relay neurons found throughout the dorsal thalamus, CMT cells assumed tonic or burst-firing modes, depending on their membrane potentials (Vm). However, they showed little evidence of the hyperpolarization-activated mixed cationic conductance (IH)-mediated inward rectification usually displayed by dorsal thalamic relay cells at hyperpolarized Vm. Two subtypes of CMT neurons were identified when comparing their responses with depolarization applied from negative potentials. Some cells generated a low-threshold spike burst followed by tonic firing, whereas others remained silent after the initial burst, irrespective of the amount of depolarizing current injected. Equal proportions of the two cell types were found among neurons retrogradely labeled from the basolateral amygdala. Their morphological properties were heterogeneous but distinct from the classical bushy relay cell type that prevails in most of the dorsal thalamus. We propose that the marginal influence of IH in CMT relative to other dorsal thalamic nuclei has significant network-level consequences. Because IH promotes the genesis of highly coherent delta oscillations in thalamocortical networks during sleep, these oscillations may be weaker or less coherent in CMT. Consequently, delta oscillations would be more easily disrupted by peripheral inputs, providing a potential mechanism for the reported role of CMT in eliciting arousal from sleep or anesthesia.


1984 ◽  
Vol 51 (6) ◽  
pp. 1220-1235 ◽  
Author(s):  
J. P. Roy ◽  
M. Clercq ◽  
M. Steriade ◽  
M. Deschenes

Intracellular recordings were performed in the lateral thalamic nuclei of cats under barbiturate anesthesia. The nature of cyclic hyperpolarizations triggered in relay cells by cortical stimulation was analyzed. These long-lasting hyperpolarizations were made of three different components. The early component, which was reversed by current and Cl injections, was identified as a Cl-dependent inhibitory postsynaptic potential (IPSP). A depolarizing hump was usually present in the depth of the long-lasting hyperpolarization. This intermediate component was identified as a voltage-dependent dendritic Ca conductance on the basis of recordings and ethylene glycol tetraacetic acid (EGTA) injections performed in relay cell dendrites. The late phase of hyperpolarization was dissociated from the early IPSP by its differential sensitivity to current and Cl injections and to conditioning tetanic stimulation. This late component was abolished by EGTA and, thus, was interpreted as a Ca-dependent K conductance increase. Activation of intrinsic somatic or dendritic conductances by current pulses never generated rhythmic hyperpolarizations in thalamic relay neurons. Oscillations appear to be imposed on these cells by synaptic inputs. It is then proposed that other thalamic neurons would have pacemaker properties and/or that oscillations would be produced in thalamic cellular pools by feedback interconnections.


2020 ◽  
Author(s):  
Andrzej T. Foik ◽  
Leo R. Scholl ◽  
Georgina A. Lean ◽  
David C. Lyon

AbstractThe pulvinar is a higher-order thalamic relay and a central component of the extrageniculate visual pathway, with input from the superior colliculus and visual cortex and output to all of visual cortex. Rodent pulvinar, more commonly called the lateral posterior nucleus (LP), consists of three highly-conserved subdivisions, and offers the advantage of simplicity in its study compared to more subdivided primate pulvinar. Little is known about receptive field properties of LP, let alone whether functional differences exist between different LP subdivisions, making it difficult to understand what visual information is relayed and what kinds of computations the pulvinar might support. Here, we characterized single-cell response properties in two V1 recipient subdivisions of rat pulvinar, the rostromedial (LPrm) and lateral (LPl), and found that a fourth of the cells were selective for orientation, compared to half in V1, and that LP tuning widths were significantly broader. Response latencies were also significantly longer and preferred size more than three times larger on average than in V1; the latter suggesting pulvinar as a source of spatial context to V1. Between subdivisons, LPl cells preferred higher temporal frequencies, whereas LPrm showed a greater degree of direction selectivity and pattern motion detection. Taken together with known differences in connectivity patterns, these results suggest two separate visual feature processing channels in the pulvinar, one in LPl related to higher speed processing which likely derives from superior colliculus input, and the other in LPrm for motion processing derived through input from visual cortex.Significance StatementThe pulvinar has a perplexing role in visual cognition as no clear link has been found between the functional properties of its neurons and behavioral deficits that arise when it is damaged. The pulvinar, called the lateral posterior nucleus (LP) in rats, is a higher order thalamic relay with input from the superior colliculus and visual cortex and output to all of visual cortex. By characterizing single-cell response properties in anatomically distinct subdivisions we found two separate visual feature processing channels in the pulvinar, one in lateral LP related to higher speed processing which likely derives from superior colliculus input, and the other in rostromedial LP for motion processing derived through input from visual cortex.


2000 ◽  
Vol 17 (1) ◽  
pp. 55-62 ◽  
Author(s):  
EION J. RAMCHARAN ◽  
JAMES W. GNADT ◽  
S. MURRAY SHERMAN

Thalamic relay cells fire in two distinct modes, burst or tonic, and the operative mode is dictated by the inactivation state of low-threshold, voltage-gated, transient (or T-type) Ca2+ channels. Tonic firing is seen when the T channels are inactivated via membrane depolarization, and burst firing is seen when the T channels are activated from a hyperpolarized state. These response modes have very different effects on the relay of information to the cortex. It had been thought that only tonic firing is seen in the awake, alert animal, but recent evidence from several species suggests that bursting may also occur. We have begun to explore this issue in macaque monkeys by recording from thalamic relay cells of unanesthetized, behaving animals. In the lateral geniculate nucleus, the thalamic relay for retinal information, we found that tonic mode dominated responses both during alert behavior as well as during sleep. We nonetheless found burst firing present during the vigilant, waking state. There was, however, considerably more burst mode firing during sleep than wakefulness. Surprisingly, we did not find the bursting during sleep to be rhythmic. We also recorded from relay cells of the somatosensory thalamus. Interestingly, not only did these somatosensory neurons exhibit much more burst mode activity than did geniculate cells, but bursting during sleep was highly rhythmic. It thus appears that the level and nature of relay cell bursting may not be constant across all thalamic nuclei.


Sign in / Sign up

Export Citation Format

Share Document