scholarly journals Cell-Type Specific Arousal-Dependent Modulation of Thalamic Activity in the Lateral Geniculate Nucleus

Author(s):  
Benedek Molnár ◽  
Péter Sere ◽  
Sándor Bordé ◽  
Krisztián Koós ◽  
Nikolett Zsigri ◽  
...  

Abstract State dependent thalamocortical activity is important for sensory coding, oscillations and cognition. The lateral geniculate nucleus (LGN) relays visual information to the cortex, but the state dependent spontaneous activity of LGN neurons in awake behaving animals remains controversial. Using a combination of pupillometry, extracellular and intracellular recordings from identified LGN neurons in behaving mice we show that thalamocortical neurons and interneurons are distinctly correlated to arousal forming two complementary coalitions. Intracellular recordings indicated that the membrane potential of LGN TC neurons was tightly correlated to fluctuations in pupil size. Inactivating the corticothalamic feedback to the LGN suppressed the arousal dependency of LGN neurons. Taken together our results show that LGN neuronal membrane potential and action potential output are dynamically linked to arousal dependent brain states in awake mice, and this might have important functional implications.

2021 ◽  
Author(s):  
Benedek Molnár ◽  
Péter Sere ◽  
Sándor Bordé ◽  
Krisztián Koós ◽  
Péter Horváth ◽  
...  

ABSTRACTState dependent thalamocortical activity is important for sensory coding, oscillations and cognition. The lateral geniculate nucleus (LGN) relays visual information to the cortex, but the state dependent spontaneous and visually evoked activity of LGN neurons in awake behaving animals remains controversial. Using a combination of pupillometry, extracellular and intracellular recordings from identified LGN neurons we show that thalamocortical neurons and interneurons are distinctly correlated to arousal forming two complementary coalitions. Intracellular recordings indicated that the membrane potential of LGN TC neurons was tightly correlated to fluctuations in pupil size. Inactivating the corticothalamic feedback to the LGN suppressed the arousal dependency of LGN neurons. Taken together our results show that LGN neuronal membrane potential and action potential output are dynamically linked to arousal dependent brain states in awake mice and this might have important functional implications.


2017 ◽  
Vol 34 ◽  
Author(s):  
CHARLES L. COX ◽  
JOSEPH A. BEATTY

AbstractIntrinsic interneurons within the dorsal lateral geniculate nucleus (dLGN) provide a feed-forward inhibitory pathway for afferent visual information originating from the retina. These interneurons are unique because in addition to traditional axodendritic output onto thalamocortical neurons, these interneurons have presynaptic dendrites that form dendrodendritic synapses onto thalamocortical neurons as well. These presynaptic dendrites, termed F2 terminals, are tightly coupled to the retinogeniculate afferents that synapse onto thalamocortical relay neurons. Retinogeniculate stimulation of F2 terminals can occur through the activation of ionotropic and/or metabotropic glutamate receptors. The stimulation of ionotropic glutamate receptors can occur with single stimuli and produces a short-lasting inhibition of the thalamocortical neuron. By contrast, activation of metabotropic glutamate receptors requires tetanic activation and results in longer-lasting inhibition in the thalamocortical neuron. The F2 terminals are predominantly localized to the distal dendrites of interneurons, and the excitation and output of F2 terminals can occur independent of somatic activity within the interneuron thereby allowing these F2 terminals to serve as independent processors, giving rise to focal inhibition. By contrast, strong transient depolarizations at the soma can initiate a backpropagating calcium-mediated potential that invades the dendritic arbor activating F2 terminals and leading to a global form of inhibition. These distinct types of output, focal versus global, could play an important role in the temporal and spatial roles of inhibition that in turn impacts thalamocortical information processing.


2015 ◽  
Vol 114 (2) ◽  
pp. 1321-1330 ◽  
Author(s):  
Christopher A. Procyk ◽  
Cyril G. Eleftheriou ◽  
Riccardo Storchi ◽  
Annette E. Allen ◽  
Nina Milosavljevic ◽  
...  

In advanced retinal degeneration loss of rods and cones leaves melanopsin-expressing intrinsically photosensitive retinal ganglion cells (ipRGCs) as the only source of visual information. ipRGCs drive non-image-forming responses (e.g., circadian photoentrainment) under such conditions but, despite projecting to the primary visual thalamus [dorsal lateral geniculate nucleus (dLGN)], do not support form vision. We wished to determine what precludes ipRGCs supporting spatial discrimination after photoreceptor loss, using a mouse model ( rd/rd cl) lacking rods and cones. Using multielectrode arrays, we found that both RGCs and neurons in the dLGN of this animal have clearly delineated spatial receptive fields. In the retina, they are typically symmetrical, lack inhibitory surrounds, and have diameters in the range of 10–30° of visual space. Receptive fields in the dLGN were larger (diameters typically 30–70°) but matched the retinotopic map of the mouse dLGN. Injections of a neuroanatomical tracer (cholera toxin β-subunit) into the dLGN confirmed that retinotopic order of ganglion cell projections to the dLGN and thalamic projections to the cortex is at least superficially intact in rd/rd cl mice. However, as previously reported for deafferented ipRGCs, onset and offset of light responses have long latencies in the rd/rd cl retina and dLGN. Accordingly, dLGN neurons failed to track dynamic changes in light intensity in this animal. Our data reveal that ipRGCs can convey spatial information in advanced retinal degeneration and identify their poor temporal fidelity as the major limitation in their ability to provide information about spatial patterns under natural viewing conditions.


2002 ◽  
Vol 19 (5) ◽  
pp. 583-592 ◽  
Author(s):  
BEN S. WEBB ◽  
CHRIS J. TINSLEY ◽  
NICK E. BARRACLOUGH ◽  
ALEXANDER EASTON ◽  
AMANDA PARKER ◽  
...  

It is well established that the responses of neurons in the lateral geniculate nucleus (LGN) can be modulated by feedback from visual cortex, but it is still unclear how cortico-geniculate afferents regulate the flow of visual information to the cortex in the primate. Here we report the effects, on the gain of LGN neurons, of differentially stimulating the extraclassical receptive field, with feedback from the striate cortex intact or inactivated in the marmoset monkey, Callithrix jacchus. A horizontally oriented grating of optimal size, spatial frequency, and temporal frequency was presented to the classical receptive field. The grating varied in contrast (range: 0–1) from trial to trial, and was presented alone, or surrounded by a grating of the same or orthogonal orientation, contained within either a larger annular field, or flanks oriented either horizontally or vertically. V1 was ablated to inactivate cortico-geniculate feedback. The maximum firing rate of LGN neurons was greater with V1 intact, but was reduced by visually stimulating beyond the classical receptive field. Large horizontal or vertical annular gratings were most effective in reducing the maximum firing rate of LGN neurons. Magnocellular neurons were most susceptible to this inhibition from beyond the classical receptive field. Extraclassical inhibition was less effective with V1 ablated. We conclude that inhibition from beyond the classical receptive field reduces the excitatory influence of V1 in the LGN. The net balance between cortico-geniculate excitation and inhibition from beyond the classical receptive field is one mechanism by which signals relayed from the retina to V1 are controlled.


eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Aurélie Pala ◽  
Carl CH Petersen

The cellular and synaptic mechanisms driving cell-type-specific function during various cortical network activities and behaviors are poorly understood. Here, we targeted whole-cell recordings to two classes of inhibitory GABAergic neurons in layer 2/3 of the barrel cortex of awake head-restrained mice and correlated spontaneous membrane potential dynamics with cortical state and whisking behavior. Using optogenetic stimulation of single layer 2/3 excitatory neurons we measured unitary excitatory postsynaptic potentials (uEPSPs) across states. During active states, characterized by whisking and reduced low-frequency activity in the local field potential, parvalbumin-expressing neurons depolarized and, albeit in a small number of recordings, received uEPSPs with increased amplitude. In contrast, somatostatin-expressing neurons hyperpolarized and reduced firing rates during active states without consistent change in uEPSP amplitude. These results further our understanding of neocortical inhibitory neuron function in awake mice and are consistent with the hypothesis that distinct genetically-defined cell classes have different state-dependent patterns of activity.


1983 ◽  
Vol 50 (4) ◽  
pp. 798-818 ◽  
Author(s):  
R. W. McCarley ◽  
O. Benoit ◽  
G. Barrionuevo

The relationship between behavioral state, discharge pattern, and discharge rate was investigated in 26 lateral geniculate nucleus (LGN) units recorded in cats in the dark during waking (W), synchronized sleep (S), and desynchronized sleep (D). A distinctive state-dependent discharge pattern was the presence of stereotyped bursts of 2-7 spikes that occurred in 63% of the units. These bursts were most frequent in S, much less frequent in D, and rarely occurred in W. Lack of association with discharge rate changes between states showed the bursting to be a true state-dependent phenomenon. A burst consisted of 2-7 spikes, with each successive interspike interval being longer than the preceding one; in the 200 ms prior to burst occurrence, discharge probability decreased markedly. This structure of burst organization suggested a model of generation wherein each burst was caused by a unitary event of varying intensity, perhaps a rebound following a hyperpolarization. Spectral and autocorrelational analyses showed bursts occurred rhythmically in three cells at a frequency of 3-4 Hz and in two cells at a frequency of 10-12 Hz, indicating a possible linkage with slow-wave generators. While the number of bursts in the various behavioral states was a state-dependent phenomena, other aspects of discharge pattern were shown to be rate dependent. To evaluate discharge pattern apart from the occurrence of bursts, a "primary event spike train" was formed; this consisted of individual spikes and the first spike of each burst. This analysis showed that, within S, the probability of burst occurrence was highest when the primary spike rate was low. Quantitative analyses showed that first-order pattern measures (the form of the interspike interval histogram, IH) were dependent on the mean interspike interval (ISI, the inverse of mean rate). This association explained 83-89% of the variance in a power series approximation of IH form. Joint interval histograms (JIH) were used to evaluate the signature of bursts and of the form of the primary spike train. As with interval histograms, the main features of the form of the primary spike JIH were dependent on the primary spike rate. Thus, we concluded that first- and second-order discharge patterns of primary events were rate dependent and not state dependent. Our data are compatible with a model where in the absence of retinal input, the frequency of LGN primary spikes over behavioral state changes is largely determined by brain stem reticular formation input.(ABSTRACT TRUNCATED AT 400 WORDS)


1999 ◽  
Vol 81 (2) ◽  
pp. 702-711 ◽  
Author(s):  
J. Julius Zhu ◽  
William W. Lytton ◽  
Jin-Tang Xue ◽  
Daniel J. Uhlrich

Intrinsic oscillation in interneurons of the rat lateral geniculate nucleus. By using the whole cell patch recording technique in vitro, we examined the voltage-dependent firing patterns of 69 interneurons in the rat dorsal lateral geniculate nucleus (LGN). When held at a hyperpolarized membrane potential, all interneurons responded with a burst of action potentials. In 48 interneurons, larger current pulses produced a bursting oscillation. When relatively depolarized, some interneurons produced a tonic train of action potentials in response to a depolarizing current pulse. However, most interneurons produced only oscillations, regardless of polarization level. The oscillation was insensitive to the bath application of a combination of blockers to excitatory and inhibitory synaptic transmission, including 30 μM 6,7-dinitroquinoxaline-2,3-dione, 100 μM (±)-2-amino-5-phosphonopentanoic acid, 20 μM bicuculline, and 2 mM saclofen, suggesting an intrinsic event. The frequency of the oscillation in interneurons was dependent on the intensity of the injection current. Increasing current intensity increased the oscillation frequency. The maximal frequency of the oscillation was 5–15 Hz for most cells, with some ambiguity caused by the difficulty of precisely defining a transition from oscillatory to regular firing behavior. In contrast, the interneuron oscillation was little affected by preceding depolarizing and hyperpolarizing pulses. In addition to being elicited by depolarizing current injections, the oscillation could also be initiated by electrical stimulation of the optic tract when the interneurons were held at a depolarized membrane potential. This suggests that interneurons may be recruited into thalamic oscillations by synaptic inputs. These results indicate that interneurons may play a larger role in thalamic oscillations than was previously thought.


1994 ◽  
Vol 11 (3) ◽  
pp. 601-617 ◽  
Author(s):  
John W. McClurkin ◽  
Lance M. Optican ◽  
Barry J. Richmond

AbstractWe studied the effect of cooling the striate cortex on parvocellular lateral geniculate nucleus (PLGN) neurons in awake monkeys. Cooling the striate cortex produced both facilitation and inhibition of the responses of all neurons, depending on the stimulus presented. Cooling the striate cortex also altered the temporal distribution of spikes in the responses of PLGN neurons. Shannon's information measure revealed that cooling the striate cortex reduced the average stimulus-related information transmitted by all PLGN neurons. The reduction in transmitted information was associated with both facilitation and inhibition of the response. Cooling the striate cortex reduced the amount of information transmitted about all of the stimulus parameters tested: pattern, luminance, spatial contrast, and sequential contrast. The effect of cooling was nearly the same for codes based on the number of spikes in the response as for codes based on their temporal distribution. The reduction in transmitted information occurred because the differences among the responses to different stimuli (signal separation) were reduced, not because the variability of the responses to individual stimuli (noise) was increased. We conclude that one function of corticogeniculate feedback is to improve the ability of PLGN neurons to discriminate among stimuli by enhancing the differences among their responses.


Sign in / Sign up

Export Citation Format

Share Document