scholarly journals The augmentation of retinogeniculate communication during thalamic burst mode

2018 ◽  
Author(s):  
Henry Alitto ◽  
Daniel L. Rathbun ◽  
Jessica J. Vandeleest ◽  
Prescott C. Alexander ◽  
W. Martin Usrey

AbstractRetinal 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.SignificanceThe 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.

2002 ◽  
Vol 357 (1428) ◽  
pp. 1695-1708 ◽  
Author(s):  
S. Murray Sherman ◽  
R. W. Guillery

The lateral geniculate nucleus is the best understood thalamic relay and serves as a model for all thalamic relays. Only 5–10% of the input to geniculate relay cells derives from the retina, which is the driving input. The rest is modulatory and derives from local inhibitory inputs, descending inputs from layer 6 of the visual cortex, and ascending inputs from the brainstem. These modulatory inputs control many features of retinogeniculate transmission. One such feature is the response mode, burst or tonic, of relay cells, which relates to the attentional demands at the moment. This response mode depends on membrane potential, which is controlled effectively by the modulator inputs. The lateral geniculate nucleus is a first–order relay, because it relays subcortical (i.e. retinal) information to the cortex for the first time. By contrast, the other main thalamic relay of visual information, the pulvinar region, is largely a higher–order relay, since much of it relays information from layer 5 of one cortical area to another. All thalamic relays receive a layer–6 modulatory input from cortex, but higher–order relays in addition receive a layer–5 driver input. Corticocortical processing may involve these corticothalamocortical ‘re–entry’ routes to a far greater extent than previously appreciated. If so, the thalamus sits at an indispensable position for the modulation of messages involved in corticocortical processing.


1996 ◽  
Vol 13 (2) ◽  
pp. 205-213 ◽  
Author(s):  
S. Murray Sherman

AbstractRelay cells of the lateral geniculate nucleus, like those of other thalamic nuclei, manifest two distinct response modes, and these represent two very different forms of relay of information to cortex. When relatively hyperpolarized, these relay cells respond with a low threshold Ca2+ spike that triggers a brief burst of conventional action potentials. These cells switch to tonic mode when depolarized, since the low threshold Ca2+ spike, being voltage dependent, is inactivated at depolarized levels. In this mode they relay information with much more fidelity. This switch can occur under the influence of afferents from the visual cortex or parabrachial region of the brain stem. It has been previously suggested that the tonic mode is characteristic of the waking state while the burst mode signals an interruption of the geniculate relay during sleep. This review surveys the key properties of these two response modes and discusses the implications of new evidence that the burst mode may also occur in the waking animal.


1994 ◽  
Vol 71 (1) ◽  
pp. 146-149 ◽  
Author(s):  
J. Cudeiro ◽  
C. Rivadulla ◽  
R. Rodriguez ◽  
S. Martinez-Conde ◽  
C. Acuna ◽  
...  

1. Using an in vivo preparation we have examined the actions of two inhibitors of nitric oxide synthase (NOS), NG-nitro-L-arginine (L-NOArg) and NG-methyl-L-arginine (L-MeArg), in the feline dorsal lateral geniculate nucleus (dLGN). We compared the responses obtained to iontophoretic application of these substances during visual stimulation with those elicited by visual stimulation alone. The effects of concurrent ejection of L-arginine (L-Arg), the normal physiological substrate of NOS, and D-arginine, the inactive isomer, were tested on these responses. 2. Extracellular application of L-NOArg and L-MeArg produced clear and repeatable effects, consisting of substantial reduction in discharge rate without affecting response selectivity, on 94% of tested cells. These effects were prevented by simultaneous application of L-Arg, which when ejected alone produced no change on visual evoked responses. 3. The data suggest that nitric oxide (NO) is necessary for the transmission of the visual input under normal visual stimulation and show a direct involvement of NO in visual information processing at the level of dLGN, suggesting that its contribution to brain mechanisms is more profound than previously thought.


1993 ◽  
Vol 10 (4) ◽  
pp. 631-642 ◽  
Author(s):  
Shao-Ming Lu ◽  
William Guido ◽  
S. Murray Sherman

AbstractWe recorded the responses of neurons from the cat’s lateral geniculate nucleus to drifting sine-wave grating stimuli both before and during electrical stimulation of the parabrachial region of the midbrain. The parabrachial region provides a mostly cholinergic input to the lateral geniculate nucleus, and our goal was to study its effect on responses of geniculate cells to visual stimulation. Geniculate neurons respond to visual stimuli in one of two modes. At relatively hyperpolarized membrane potentials, low threshold (LT) Ca2+ spikes are activated, leading to high-frequency burst discharges (burst mode). At more depolarized levels, the low threshold Ca2+ spike is inactivated, permitting a more tonic response (relay or tonic mode). During our intracellular recordings of geniculate cells, we found that, at initially hyperpolarized membrane potentials, LT spiking in response to visual stimulation was pronounced, but that parabrachial activation abolished this LT spiking and associated burst discharges. Coupled with the elimination of LT spiking, parabrachial activation also led to a progressive increase in tonic responsiveness. Parabrachial activation thus effectively switched the responses to visual stimulation of geniculate neurons from the burst to relay mode. Accompanying this switch was a gradual depolarization of resting membrane potential by about 5–10 mV and a reduction in the hyperpolarization that normally occurs in response to the inhibitory phase of the visual stimulus. Presumably, the membrane depolarization was sufficient to inactivate the LT spikes. We were able to extend and confirm our intracellular observations on the effects of parabrachial activation to a sample of cells recorded extracellularly. This was made possible by adopting empirically determined criteria to distinguish LT bursts from tonic responses solely on the basis of the temporal pattern of action potentials. During parabrachial activation, every cell responded only in the relay mode, an effect that corresponds to our intracellular observations. We quantified the effects of parabrachial activation on various response measures. The fundamental Fourier response amplitude (Fl) was calculated separately for the total response, the tonic response component, and the LT burst component. Parabrachial activation resulted in an increased Fl amplitude for the total response. This increase was due to an increase in the tonic response component. For a subset of cells showing epochs of LT bursting, parabrachial activation concurrently reduced LT bursting and increased the amplitude of the tonic response. Parabrachial activation, by eliminating LT bursting, also caused cells to respond with more linearity. By keeping geniculate cells in the relay mode, the parabrachial region serves to maintain a more linear retinogeniculate transfer of information to cortex, and this may be important for detailed analysis of visual targets. However, when a geniculate neuron becomes hyperpolarized, as may occur during states of visual inattention, it would not respond well to visual stimuli without the sort of nonlinear amplification provided by the LT spike. Thus, the LT spike may permit hyperpolarized cells to relay to cortex the presence of a potentially salient or dangerous stimulus, but this is done at the expense of linearity. This may serve as a sort of “wake-up call” that redirects attention to a particular stimulus and eventually enhances activity of appropriate parabrachial inputs to switch the critical geniculate neurons into the relay mode.


2000 ◽  
Vol 17 (2) ◽  
pp. 187-196 ◽  
Author(s):  
JOKUBAS ZIBURKUS ◽  
MARTHA E. BICKFORD ◽  
WILLIAM GUIDO

In normal adult cats, a monoclonal antibody directed toward the NR-1 subunit of the N-methyl-d-aspartate (NMDA) receptor (Pharmingen, clone 54.1) produced dense cellular and neuropil labeling throughout all layers of the lateral geniculate nucleus (LGN) and adjacent thalamic nuclei, including the thalamic reticular, perigeniculate, medial intralaminar, and ventral lateral geniculate nuclei. Cellular staining revealed well-defined somata, and in some cases proximal dendrites. NMDAR-1 cell labeling was also evident in the LGN of early postnatal kittens, suggesting that developing LGN cells possess this receptor subunit at or before eye opening. Within the A-layers of the adult LGN, staining encompassed a wide range of soma sizes. Soma size comparisons of NMDAR-1 stained cells with those stained with an antibody directed toward a nonphosphorylated neurofilament protein (SMI-32), which selectively stains Y-relay cells (Bickford et al., 1998), or an antibody to glutamic acid decarboxylase (GAD), which stains for GABAergic interneurons, suggested that NMDA receptors are utilized by relay cells and interneurons. NMDAR-1 staining was also observed in the LGN of cats with early monocular lid suture. Although labeling was apparent in both deprived and nondeprived A-layers of LGN, the distribution of soma sizes was significantly different. In the deprived A-layers of LGN, staining was limited to small- and medium-sized cells. Cells with relatively large soma were lacking. However, cell density measurements as well as soma size comparisons with cells stained for Nissl substance suggested these differences were due to deprivation-induced cell shrinkage and not to a loss of NMDAR-1 staining in Y-cells. Taken together, these results suggest that NMDA receptors are utilized by both relay cells and interneurons in LGN and that alterations in early visual experience do not necessarily affect the expression of NMDA receptors in the LGN.


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.


1996 ◽  
Vol 76 (3) ◽  
pp. 1800-1816 ◽  
Author(s):  
D. W. Godwin ◽  
J. W. Vaughan ◽  
S. M. Sherman

1. Metabotropic glutamate receptors (mGluRs) on relay cells of the lateral geniculate nucleus appear to be activated exclusively by cortical inputs. We thus sought to manipulate these receptors in an effort to gain insight into the possible role of the corticogeniculate pathway. We used in vivo recording and pharmacological techniques in cats to activate or inactivate these receptors on geniculate neurons while analyzing their response properties. 2. Iontophoretic application of the mGluR agonist 1-amino-cyclopentane-1,3-dicarboxylic acid (ACPD) to X and Y cells in the geniculate A laminae diminished or abolished burst activity characteristic of low-threshold Ca2+ spikes. This was accompanied by pronounced changes in the visual response, including a decrease in signal detectability as measured with receiver operating characteristic curves. 3. ACPD effects appear specific to mGluRs, because a specific antagonist of ionotropic glutamate receptors (iGluRs) failed to affect the ACPD-evoked responses, and antagonists of ACPD failed to affect iGluR-mediated responses. We found that 3,5-dihydroxyphenylglycine, an agonist reported to be specific for phosphatidylinositol (PI)-linked mGluRs, had effects similar to those of ACPD, implying that these effects are mediated by PI-coupled mGluRs. Furthermore, antagonists reported to be effective against PI-linked mGluRs were effective in antagonizing the ACPD-mediated effects, and substances reported to be agonists to mGluRs coupled to the adenosine 3',5'-cyclic monophosphate cascade did not affect neuronal responses on their own. These data, when added to our preliminary anatomic data, indicate that the receptor responsible for the observed effects may be mGluR1, or a functionally equivalent mGluR. 4. Activation of mGluRs produces changes in geniculate relay cell activity consistent with depolarization of these cells seen during in vitro studies. Such membrane depolarization has been shown to control the activation state of a voltage-dependent Ca2+ conductance, and this, in turn, determines whether the relay cell fires in tonic or burst mode. Our data show that application of ACPD produces a shift in response mode from burst to tonic. Because response mode is an important characteristic of the geniculate relay and because the activation state of certain mGluRs, which helps determine response mode may be controlled by corticogeniculate input, we conclude that an important function of this input is to provide a visuotopically discrete transition from burst to tonic response mode.


1998 ◽  
Vol 79 (2) ◽  
pp. 922-936 ◽  
Author(s):  
Daeyeol Lee ◽  
Joseph G. Malpeli

Lee, Daeyeol and Joseph G. Malpeli. Effects of saccades on the activity of neurons in the cat lateral geniculate nucleus. J. Neurophysiol. 79: 922–936, 1998. Effects of saccades on individual neurons in the cat lateral geniculate nucleus (LGN) were examined under two conditions: during spontaneous saccades in the dark and during stimulation by large, uniform flashes delivered at various times during and after rewarded saccades made to small visual targets. In the dark condition, a suppression of activity began 200–300 ms before saccade start, peaked ∼100 ms before saccade start, and smoothly reversed to a facilitation of activity by saccade end. The facilitation peaked 70–130 ms after saccade end and decayed during the next several hundred milliseconds. The latency of the facilitation was related inversely to saccade velocity, reaching a minimum for saccades with peak velocity >70–80°/s. Effects of saccades on visually evoked activity were remarkably similar: a facilitation began at saccade end and peaked 50–100 ms later. When matched for saccade velocity, the time courses and magnitudes of postsaccadic facilitation for activity in the dark and during visual stimulation were identical. The presaccadic suppression observed in the dark condition was similar for X and Y cells, whereas the postsaccadic facilitation was substantially stronger for X cells, both in the dark and for visually evoked responses. This saccade-related regulation of geniculate transmission appears to be independent of the conditions under which the saccade is evoked or the state of retinal input to the LGN. The change in activity from presaccadic suppression to postsaccadic facilitation amounted to an increase in gain of geniculate transmission of ∼30%. This may promote rapid central registration of visual inputs by increasing the temporal contrast between activity evoked by an image near the end of a fixation and that evoked by the image immediately after a saccade.


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