Reciprocal inhibition and slow calcium decay in perigeniculate interneurons explain changes of spontaneous firing of thalamic cells caused by cortical inactivation (original) (raw)
Related papers
Acta Neurobiologiae Experimentalis, 2012
The role of cortical feedback in the thalamocortical processing loop has been extensively investigated over the last decades. With an exception of several cases, these searches focused on the cortical feedback exerted onto thalamo-cortical relay (TC) cells of the dorsal lateral geniculate nucleus (LGN). In a previous, physiological study, we showed in the cat visual system that cessation of cortical input, despite decrease of spontaneous activity of TC cells, increased spontaneous firing of their recurrent inhibitory interneurons located in the perigeniculate nucleus (PGN). To identify mechanisms underlying such functional changes we conducted a modeling study in NEURON on several networks of point neurons with varied model parameters, such as membrane properties, synaptic weights and axonal delays. We considered six network topologies of the retino-geniculo-cortical system. All models were robust against changes of axonal delays except for the delay between the LGN feed-forward interneuron and the TC cell. The best representation of physiological results was obtained with models containing reciprocally connected PGN cells driven by the cortex and with relatively slow decay of intracellular calcium. This strongly indicates that the thalamic reticular nucleus plays an essential role in the cortical influence over thalamo-cortical relay cells while the thalamic feed-forward interneurons are not essential in this process. Further, we suggest that the dependence of the activity of PGN cells on the rate of calcium removal can be one of the key factors determining individual cell response to elimination of cortical input.
BMC Neuroscience, 2013
The role of cortical feedback in the thalamocortical processing loop has been extensively investigated over the last decades. With an exception of several cases, these searches focused on the cortical feedback exerted onto thalamo-cortical relay (TC) cells of the dorsal lateral geniculate nucleus (LGN). In a previous, physiological study, we showed in the cat visual system that cessation of cortical input, despite decrease of spontaneous activity of TC cells, increased spontaneous firing of their recurrent inhibitory interneurons located in the perigeniculate nucleus (PGN). To identify mechanisms underlying such functional changes we conducted a modeling study in NEURON on several networks of point neurons with varied model parameters, such as membrane properties, synaptic weights and axonal delays. We considered six network topologies of the retino-geniculo-cortical system. All models were robust against changes of axonal delays except for the delay between the LGN feed-forward interneuron and the TC cell. The best representation of physiological results was obtained with models containing reciprocally connected PGN cells driven by the cortex and with relatively slow decay of intracellular calcium. This strongly indicates that the thalamic reticular nucleus plays an essential role in the cortical influence over thalamo-cortical relay cells while the thalamic feed-forward interneurons are not essential in this process. Further, we suggest that the dependence of the activity of PGN cells on the rate of calcium removal can be one of the key factors determining individual cell response to elimination of cortical input.
Inhibitory Interactions Between Perigeniculate GABAergic Neurons
Journal of …, 1997
Perigeniculate neurons form an interactive sheet of cells that inhibit one another as well as thalamocortical neurons in the dorsal lateral geniculate nucleus (LGNd). The inhibitory influence of the GABAergic neurons of the perigeniculate nucleus (PGN) onto other PGN neurons was examined with intracellular recordings in vitro. Intracellular recordings from PGN neurons during the generation of spindle waves revealed barrages of EPSPs and IPSPs. The excitation of local regions of the PGN with the local application of glutamate resulted in activation of IPSPs in neighboring PGN neurons. These IPSPs displayed an average reversal potential of Ϫ77 mV and were blocked by application of bicuculline methiodide or picrotoxin, indicating that they are mediated by GABA A receptors. In the presence of GABA A receptor blockade, the activation of PGN neurons with glutamate could result in slow IPSPs that were mediated by GABA B receptors in a subset (40%) of cells. Similarly, application of specific agonists muscimol and baclofen demonstrated that PGN neurons possess both functional GABA A and GABA B receptors. Examination of the axon arbors of biocytin-filled PGN neurons often revealed the presence of beaded axon collaterals within the PGN, suggesting that this may be an anatomical substrate for PGN to PGN inhibition.
The Journal of Physiology, 2004
The feedback excitation from the primary visual cortex to principal cells in the dorsal lateral geniculate nucleus (dLGN) is markedly enhanced with firing frequency. This property presumably reflects the ample short-term plasticity at the corticogeniculate synapse. The present study aims to explore corticogeniculate excitatory postsynaptic currents (EPSCs) evoked by brief trains of stimulation with whole-cell patch-clamp recordings in dLGN slices from DA-HAN rats. The EPSCs rapidly increased in amplitude with the first two or three impulses followed by a more gradual growth. A double exponential function with time constants 39 and 450 ms empirically described the growth for 5-25 Hz trains. For lower train frequencies (down to 1 Hz) a third component with time constant 4.8 s had to be included. The different time constants are suggested to represent fast and slow components of facilitation and augmentation. The time constant of the fast component changed with the extracellular calcium ion concentration as expected for a facilitation mechanism involving an endogenous calcium buffer that is more efficiently saturated with larger calcium influx. Concerning the function of the corticogeniculate feedback pathway, the different components of short-term plasticity interacted to increase EPSC amplitudes on a linear scale to firing frequency in the physiological range. This property makes the corticogeniculate synapse well suited to function as a neuronal amplifier that enhances the thalamic transfer of visual information to the cortex.
The Journal of Physiology, 2000
1. Calcium dynamics associated with a single action potential (AP) were studied in single boutons of the axonal arbor of layer 2Ï3 pyramidal cells in the neocortex of young (P14-16) rats. We used fluorescence imaging with two-photon excitation and Ca¥-selective fluorescence indicators to measure volume-averaged Ca¥ signals. These rapidly reached a peak (in about 1 ms) and then decayed more slowly (tens to hundreds of milliseconds). 2. Single APs and trains of APs reliably evoked Ca¥ transients in en passant boutons located on axon collaterals in cortical layers 2Ï3, 4 and 5, indicating that APs propagate actively and reliably throughout the axonal arbor. Branch point failures are unlikely to contribute to differences in synaptic efficacy and reliability in the connections made by layer 2Ï3 pyramidal cells. 3. AP-evoked Ca¥ transients in boutons were mediated by voltage-dependent Ca¥ channels (VDCCs), predominantly by the PÏQ-and N-subtypes. 4. Ca¥ transients were, on average, of significantly larger amplitude in boutons than in the flanking segments of the axon collateral. Large amplitude Ca¥ transients in boutons were spatially restricted to within û 3 ìm of axonal length. 5. Single AP-evoked Ca¥ transients varied up to 10-fold across different boutons even if they were located on the same axon collateral. In contrast, variation of Ca¥ transients evoked by successive APs in a given single bouton was small (coefficient of variation, c.v. û 0•21). 6. Amplitudes of AP-evoked Ca¥ signals did not correlate with the distance of boutons from the soma. In contrast, AP-evoked Ca¥ signals in spines of basal dendrites decreased slightly (correlation coefficient, r 2 = −0•27) with distance from the soma. 7. Measurements with the low-affinity Ca¥ indicator Magnesium Green suggest that the volume-averaged residual free [Ca¥]é in a bouton increases on average by 500 nÒ following a single AP. Higher concentrations of indicator caused, on average, a decrease in the amplitude and an increase in the decay time constant of Ca¥ transients. Assuming a singlecompartment model the concentration dependence of decay time constants suggests a low endogenous Ca¥ binding ratio close to 140, indicating that of the total Ca¥ influx (•2 fC) less than 1 % remained free. 8. The indicator concentration dependence of decay time constants further suggests that the residual free Ä[Ca¥]i associated with an AP decays with a time constant of about 60 ms (35°C) reflecting a high Ca¥ extrusion rate of about 2600 s¢. 9. The results show that AP-evoked volume-averaged Ca¥ transients in single boutons are evoked reliably and, on average, have larger amplitudes than Ca¥ transients in other subcellular compartments of layer 2Ï3 pyramidal cells. A major functional signature is the large variation in the amplitude of Ca¥ transients between different boutons. This could indicate that local interactions between boutons and different target cells modify the spatiotemporal Ca¥ dynamics in boutons and cause target cell-specific differences in their transmitter release properties.
The Journal of Physiology, 2002
To investigate paired pulse facilitation of corticogeniculate EPSCs, whole-cell patch-clamp recordings were made from principal cells in the rat dorsal lateral geniculate nucleus (dLGN) in vitro. Thalamic slices, oriented so that both corticogeniculate and retinogeniculate axons could be stimulated, were cut from young (16-to 37-day-old) DA-HAN rats. Corticogeniculate EPSCs displayed pronounced paired pulse facilitation at stimulus intervals up to 400 ms. The facilitation had a fast and a slow component of decay with time constants of 12 ± 7 and 164 ± 47 ms (means ± S.D.), respectively. Maximum paired pulse ratio (EPSC 2 w EPSC 1 _1) was 3.7 ± 1.1 at the 20-30 ms interval. Similar to other systems, the facilitation was presynaptic. Retinogeniculate EPSCs recorded in the same dLGN cells displayed paired pulse depression at intervals up to at least 700 ms. The two types of EPSCs differed in their calcium response curves. At normal [Ca 2+ ] o , the corticogeniculate synapse functioned over the early rising part of a Hill function, while the retinogeniculate synapse operated over the middle and upper parts of the curve. The paired pulse ratio of corticogeniculate EPSCs was maximal at physiological [Ca 2+ ] o. The facilitation is proposed to have an important role in the function of the corticogeniculate circuit as a neuronal amplifier.
Journal of Neurophysiology, 2013
Andolina IM, Jones HE, Sillito AM. Effects of cortical feedback on the spatial properties of relay cells in the lateral geniculate nucleus. Feedback connections to earlylevel sensory neurons have been shown to affect many characteristics of their neural response. Because selectivity for stimulus size is a fundamental property of visual neurons, we examined the summation tuning and discretely mapped receptive field (RF) properties of cells in the lateral geniculate nucleus (LGN) both with and without feedback from visual cortex. Using extracellular recording in halothaneanesthetized cats, we used small luminance probes displaced in Cartesian coordinates to measure discrete response area, and optimal sinusoidal gratings of varying diameter to estimate preferred optimal summation size and level of center-surround antagonism. In conditions where most cortical feedback was pharmacologically removed, discretely mapped RF response areas showed an overall significant enlargement for the population compared with control conditions. A switch to increased levels of burst firing, spatially displaced from the RF center, suggested this was mediated by changes in excitatoryinhibitory balance across visual space. With the use of coextensive stimulation, there were overall highly significant increases in the optimal summation size and reduction of surround antagonism with removal of cortical feedback in the LGN. When fitted with a difference-of-Gaussian (DOG) model, changes in the center size, center amplitude, and surround amplitude parameters were most significantly related to the removal of cortical feedback. In summary, corticothalamic innervation of the visual thalamus can modify spatial summation properties in LGN relay cells, an effect most parsimoniously explained by changes in the excitatory-inhibitory balance. summation; receptive field; visual cortex; corticothalamic; corticofugal ONE OF THE EARLIEST IDENTIFIED characteristics of receptive fields (RFs) in the visual system is selectivity for stimulus size. When a light disc is centered over a RF and enlarged, cells show first an increase in response magnitude (summation) and then, in many cases, a reduction (suppression) beyond a certain diameter Hartline 1940 Fig. 3; Hubel and Wiesel 1962). The interaction of increasing diameter is broadly antagonistic, and a general model of the RF consisting of a central Gaussian excitatory zone and a coextensive Gaussian suppressive zone was first proposed by for retinal ganglion cells. This difference-of-Gaussian (DOG) model and its derivatives have since been used across species to successfully model responses in visual neurons from retina to visual cortex for a range of stimuli Cai et al. 1997; DeAngelis et al. 1994; Einevoll and Plesser 2005, 2012; Enroth-Cugell and Robson 1966; Kremers et al. 2001; Nolt et METHODS Experiments were performed on anesthetized (70% N 2 O, 30% O 2 , 0.1-0.5% halothane), paralyzed (10 mg·kg Ϫ1 ·h Ϫ1 gallamine triethiodide) cats as described in detail elsewhere (Cudeiro and Sillito 1996). We took data from 12 control cats and 11 cats with cortical feedback to the LGN pharmacologically inactivated. All procedures were in accordance with British Home Office license requirements and were Address for reprint requests and other correspondence: I. M. Andolina, . Nature and interaction of signals from the receptive field center and surround in macaque V1 neurons. J Neurophysiol 88: 2530 -2546, 2002. Cleland BG, Lee BB. A comparison of visual responses of cat lateral geniculate nucleus neurones with those of ganglion cells afferent to them. J Physiol 369: 249 -268, 1985. Crunelli V, Lightowler S, Pollard CE. A T-type Ca 2ϩ current underlies low-threshold Ca 2ϩ potentials in cells of the cat and rat lateral geniculate nucleus. J Physiol 413: 543-561, 1989. Cudeiro J, Sillito AM. Spatial frequency tuning of orientation-discontinuitysensitive corticofugal feedback to the cat lateral geniculate nucleus. J Physiol 490: 481-492, 1996. de Labra C, Rivadulla C, Grieve K, Mariño J, Espinosa N, Cudeiro J. Changes in visual responses in the feline dLGN: selective thalamic suppression induced by transcranial magnetic stimulation of V1. Cereb Cortex 17: 1376 -1385, 2007. DeAngelis GC, Freeman RD, Ohzawa I. Length and width tuning of neurons in the cat's primary visual cortex. J Neurophysiol 71: 347-374, 1994. Deleuze C, Huguenard JR. Distinct electrical and chemical connectivity maps in the thalamic reticular nucleus: potential roles in synchronization and sensation. J Neurosci 26: 8633-8645, 2006. Derrington AM, Felisberti F. Peripheral shift reduces visual sensitivity in cat geniculate neurones. Vis Neurosci 15: 875-880, 1998. Destexhe A, Sejnowski TJ. The initiation of bursts in thalamic neurons and the cortical control of thalamic sensitivity. Philos Trans R Soc Lond B Biol Sci 357: 1649 -1657, 2002. Einevoll GT, Plesser HE. Extended difference-of-Gaussians model incorporating cortical feedback for relay cells in the lateral geniculate nucleus of cat. Cogn Neurodyn 6: 307-324, 2012. Einevoll GT, Plesser HE. Response of the difference-of-Gaussians model to circular drifting-grating patches. Vis Neurosci 22: 437-446, 2005. Enroth-Cugell C, Robson J. The contrast sensitivity of retinal ganglion cells of the cat. J Physiol 187: 517-552, 1966. Eriş ir A, Van Horn SC, Sherman SM. Relative numbers of cortical and brainstem inputs to the lateral geniculate nucleus. Proc Natl Acad Sci USA 94: 1517-1520, 1997. Funke K, Eysel UT. Inverse correlation of firing patterns of single topographically matched perigeniculate neurons and cat dorsal lateral geniculate relay cells. Vis Neurosci 15: 711-729, 1998. Golshani P, Liu XB, Jones EG. Differences in quantal amplitude reflect GluR4-subunit number at corticothalamic synapses on two populations of thalamic neurons. Proc Natl Acad Sci USA 98: 4172-4177, 2001. Hartline HK. The effects of spatial summation in the retina on the excitation of the fibers of the optic nerve.