Efficacy of Thalamocortical and Intracortical Synaptic Connections (original) (raw)
The Journal of neuroscience : the official journal of the Society for Neuroscience, 2016
Comparative physiological and anatomical studies have greatly advanced our understanding of sensory systems. Many lines of evidence show that the murine lateral geniculate nucleus (LGN) has unique attributes, compared with other species such as cat and monkey. For example, in rodent, thalamic receptive field structure is markedly diverse, and many cells are sensitive to stimulus orientation and direction. To explore shared and different strategies of synaptic integration across species, we made whole-cell recordings in vivo from the murine LGN during the presentation of visual stimuli, analyzed the results with different computational approaches, and compared our findings with those from cat. As for carnivores, murine cells with classical center-surround receptive fields had a "push-pull" structure of excitation and inhibition within a given On or Off subregion. These cells compose the largest single population in the murine LGN (∼40%), indicating that push-pull is key in ...
Thalamocortical Specificity and the Synthesis of Sensory Cortical Receptive Fields
Alonso, Jose-Manuel and Harvey A. Swadlow. Thalamocortical specificity and the synthesis of sensory cortical receptive fields. . A persistent and fundamental question in sensory cortical physiology concerns the manner in which receptive fields of layer-4 neurons are synthesized from their thalamic inputs. According to a hierarchical model proposed more than 40 years ago, simple receptive fields in layer 4 of primary visual cortex originate from the convergence of highly specific thalamocortical inputs (e.g., geniculate inputs with ON-center receptive fields overlap the ON subregions of layer 4 simple cells).
Neuron, 1999
connections from thalamus to cortex are significantly of each input to the construction of receptive field propmore effective than IC connections; although quantal erties in primary sensory areas of cortex is unclear. This size is the same in the two tracts, TC connections have issue has been intensively investigated for orientation a higher innervation ratio and release probability than selectivity in visual cortex. Some studies have con-IC connections. cluded that spatially aligned TC inputs alone account for orientation selectivity, while others suggest that recurrent IC circuits provide essential enhancement of Results weak TC inputs (for discussions, see Hubel and Wiesel, 1962; Douglas et al., 1995; Reid and Alonso, 1995, 1996; Our basic strategy was to record from single spiny neurons of the primary somatosensory (barrel) cortex in vitro and independently measure the properties of TC and IC inputs to each cell (Gil and Amitai, 1996; Gil et ‡ To whom correspondence should be addressed (e-mail: barry_ connors@brown.edu). al., 1997). The biocytin-stained cells we recovered (n ϭ Neuron 386 Gil and Amitai, 1996; Gil et al., 1997). Crossed paired pulses were References used to verify that stimuli of one tract were not contaminated by activation of axons from the other tract (Gil et al., 1997). In some Abdul-Ghani, M.A., Valiante, T.A., and Pennefather, P.S. (1996). Sr 2ϩ and quantal events at excitatory synapses between mouse hippo-experiments, biocytin (0.1%) was included in the pipette solution, and the slices were processed by standard avidin-biotin-peroxidase campal neurons in culture. J. Physiol. (Lond.) 495, 113-125. procedures (Horikawa and Armstrong, 1988). Agmon, A., and Connors, B.W. (1991). Thalamocortical responses The transmitter receptor blockers bicuculline methiodide (BMI, 5 of mouse somatosensory (barrel) cortex in vitro. Neuroscience 41, M; RBI), D,L-2-amino-5-phosphonovalerate (APV, 30 M; RBI), 6,7-365-379. dinitroquinoxaline-2,3-dione (DNQX, 15 M; RBI), and MK-801 (40 Agmon, A., and Connors, B.W. (1992). Correlation between intrinsic M) were added to the perfusate. In some experiments, Ca 2ϩ was firing patterns and thalamocortical synaptic responses of neurons replaced by 4 mM [Sr] and [Mg] was raised to 4 mM, and the solution in mouse barrel cortex. J. Neurosci. 12, 319-329. was introduced at least 15 min before recording started. Ahmed, B., Anderson, J.C., Douglas, R.J., Martin, K.A.C., and Nelson, J.C. (1994). Polyneuronal innervation of spiny stellate neurons in cat visual cortex. J. Comp. Neurol. 341, 39-49. Minimal Stimulation Bear, M.F., and Malenka, R.C. (1994). Synaptic plasticity: LTP and During minimal-stimulation experiments, we used a bathing solution LTD. Curr. Opin. Neurobiol. 4, 389-399. containing 3 mM [Ca] and 1 mM [Mg]. To apply as focal a stimulus as possible, we developed a homemade stimulating electrode from Buhl, E.H., Tamas, G., Szilagyi, T., Stricker, C., Paulsen, O., and 2 mm outside diameter glass tubing with a cross section. The Somogyi, P. (1997). Effect, number and location of synapses made glass was pulled in a conventional two-stage puller to a tip size of by single pyramidal cells onto aspiny interneurones of cat visual Ͻ10 m in diameter. Each side of the tubing was filled with ACSF, cortex. J. Physiol. (Lond.) 500, 689-713. and electrical contact was made through two AgCl wires pushed Calverley, R.K.S., and Jones, D.G. (1990). Contribution of dendritic as close as possible to the tip. The tip was gently pushed into the spines and perforated synapses to synaptic plasticity. Brain Res. slice, and low stimulus intensities (Ͻ10 A, 0.1-0.2 ms duration) Rev. 15, 215-249. were used to minimize the area of activation; such stimuli always Castro-Alamancos, M.A., and Connors, B.W. (1996). Short-term failed to evoke a measurable field potential near the recorded cortiplasticity of a thalamocortical pathway dynamically modulated by cal neuron. The criteria for single-axon stimulation were: (1) all-orbehavioral state. Science 272, 274-277. none synaptic events, (2) little or no variation in EPSC latencies, (3) Castro-Alamancos, M.A., and Connors, B.W. (1997). Distinct forms a small change in the stimulus intensity did not change the mean of short-term plasticity at excitatory synapses of hippocampus and size or shape of the EPSC, and (4) lowering stimulus intensities by neocortex. Proc. Natl. Acad. Sci. USA 94, 4161-4166. 10%-20% resulted in complete failure to evoke EPSCs. Typically, 150-200 trials were obtained from each cell. Chance, F.S., Nelson, S.B., and Abbott, L.F. (1998). Synaptic depression and temporal response characteristics of V1 cells. J. Neurosci. 18, 4785-4799. Data Analysis Chung, S., and Ferster, D. (1998). Strength and orientation tuning Unitary EPSPs or EPSCs and spontaneous events were detected of the thalamic input to simple cells revealed by electrically evoked by threshold and by the first derivative (Malgaroli and Tsien, 1992; cortical suppression. Neuron 20, 1177-1189. Oliet et al., 1996) and were inspected by eye with software pro-Crair, M.C., and Malenka, R.C. (1995). A critical period for long-term grammed under the LabView environment (National Instruments). potentiation at thalamocortical synapses. Nature 375, 325-328. Baseline noise was measured during a 5 ms time window preceding Debanne, D., Guerineau, N.C., Gahwiler, B.H., and Thompson, S.M. each measured event. The signal-to-noise ratio for quantal EPSCs (1996). Paired-pulse facilitation and depression at unitary synapses was calculated as the ratio between the mean event amplitude and in rat hippocampus: quantal fluctuation affects subsequent release. the standard deviation of the noise, and was very similar for both J. Physiol. (Lond.) 491, 163-175. tracts (9.2 for the TC tract and 9.4 for the IC tract). Thus, there is no reason to suspect that we have missed a substantial number of Deuchars, J., West, D.C., and Thomson, A.M. (1995). Relationships events in either pathway or that events were differentially missed. between morphology and physiology of pyramid-pyramid single The progressive block of NMDA EPSCs in the presence of MKaxon connections in rat neocortex in vitro. J. Physiol. (Lond.) 478, 801 was fitted with a biexponential curve, using a simplex fitting 423-435. algorithm to minimize 2 (Kullmann et al., 1996). For analysis of Dobrunz, L.E., and Stevens, C.F. (1997). Heterogeneity of release EPSC/P amplitude distributions, a sum of Gaussian functions was probability, facilitation, and depletion at central synapses. Neuron fitted to the histograms by the method of least squares (Paulsen 18, 995-1008. and Heggelund, 1994). Statistical comparisons were made with the Dodge, F.A., Miledi, R., and Rahamimoff, R. (1969). Sr 2ϩ and quantal Wilcoxon test for paired samples, the Mann-Whitney test for unrelease of transmitter at the neuromuscular junction. J. Physiol. 200, paired samples, or t tests. The coefficient of variation (CV) was 267-284. defined as ( s 2 Ϫ n 2 ) 1/2 / s , where s and n are the variances of the Douglas, R.J., Koch, C., Mahowald, M., Martin, K.A.C., and Suarez, synaptic measurements and noise, respectively, and s is the mean H.H. (1995). Recurrent excitation in neocortical circuits. Science 269, synaptic size. The comparison between the TC and the IC cumula-981-985. tive distributions was made using the resampling (bootstrapping) Ferster, D., Chung, S., and Wheat, H. (1996). Orientation selectivity method (Van der Kloot, 1996). Unless specified, data are reported of thalamic input to simple cells of cat visual cortex. Nature 380, as mean Ϯ SD. 249-252. Fleidervish, I.A., Binshtok, A.M., and Gutnick, M.J. (1998). Function-
Target-specific properties of thalamocortical synapses onto layer 4 of mouse primary visual cortex
The Journal of neuroscience : the official journal of the Society for Neuroscience, 2014
In primary sensory cortices, thalamocortical (TC) inputs can directly activate excitatory and inhibitory neurons. In vivo experiments in the main input layer (L4) of primary visual cortex (V1) have shown that excitatory and inhibitory neurons have different tuning properties. The different functional properties may arise from distinct intrinsic properties of L4 neurons, but could also depend on cell type-specific properties of the synaptic inputs from the lateral geniculate nucleus of the thalamus (LGN) onto L4 neurons. While anatomical studies identified LGN inputs onto both excitatory and inhibitory neurons in V1, their synaptic properties have not been investigated. Here we used an optogenetic approach to selectively activate LGN terminal fields in acute coronal slices containing V1, and recorded monosynaptic currents from excitatory and inhibitory neurons in L4. LGN afferents made monosynaptic connections with pyramidal (Pyr) and fast-spiking (FS) neurons. TC EPSCs on FS neurons...
Synaptic Correlates of Low-Level Perception in V1
The Journal of neuroscience : the official journal of the Society for Neuroscience, 2016
The computational role of primary visual cortex (V1) in low-level perception remains largely debated. A dominant view assumes the prevalence of higher cortical areas and top-down processes in binding information across the visual field. Here, we investigated the role of long-distance intracortical connections in form and motion processing by measuring, with intracellular recordings, their synaptic impact on neurons in area 17 (V1) of the anesthetized cat. By systematically mapping synaptic responses to stimuli presented in the nonspiking surround of V1 receptive fields, we provide the first quantitative characterization of the lateral functional connectivity kernel of V1 neurons. Our results revealed at the population level two structural-functional biases in the synaptic integration and dynamic association properties of V1 neurons. First, subthreshold responses to oriented stimuli flashed in isolation in the nonspiking surround exhibited a geometric organization around the preferre...
Functional Properties of Synaptic Transmission in Primary Sense Organs
Journal of Neuroscience, 2009
Sensory receptors transduce physical stimuli in the environment into neural signals that are interpreted by the brain. Although considerable attention has been given to how the sensitivity and dynamic range of sensory receptors is established, peripheral synaptic interactions improve the fidelity with which receptor output is transferred to the brain. For instance, synapses in the retina, cochlea, and primary olfactory system use mechanisms that fine-tune the responsiveness of postsynaptic neurons and the dynamics of exocytosis; these permit microcircuit interactions to encode efficiently the output of sensory receptors with the fidelity and dynamic range necessary to extract the salient features of the physical stimuli. The continuous matching of presynaptic and postsynaptic responsiveness highlight how the primary sensory organs have been optimized and can be modulated to resolve sparse sensory signals and to encode the entire range of receptor output.
Synaptic targets of thalamic reticular nucleus terminals in the visual thalamus of the cat
Journal of Comparative Neurology, 2001
A major inhibitory input to the dorsal thalamus arises from neurons in the thalamic reticular nucleus (TRN), which use gamma-aminobutyric acid (GABA) as a neurotransmitter. We examined the synaptic targets of TRN terminals in the visual thalamus, including the A lamina of the dorsal lateral geniculate nucleus (LGN), the medial interlaminar nucleus (MIN), the lateral posterior nucleus (LP), and the pulvinar nucleus (PUL). To identify TRN terminals, we injected biocytin into the visual sector of the TRN to label terminals by anterograde transport. We then used postembedding immunocytochemical staining for GABA to distinguish TRN terminals as biocytin-labeled GABA-positive terminals and to distinguish the postsynaptic targets of TRN terminals as GABA-negative thalamocortical cells or GABA-positive interneurons. We found that, in all nuclei, the TRN provides GABAergic input primarily to thalamocortical relay cells (93-100%). Most of this input seems targeted to peripheral dendrites outside of glomeruli. The TRN does not appear to be a significant source of GABAergic input to interneurons in the visual thalamus. We also examined the synaptic targets of the overall population of GABAergic axon terminals (F1 profiles) within these same regions of the visual thalamus and found that the TRN contacts cannot account for all F1 profiles. In addition to F1 contacts on the dendrites of thalamocortical cells, which presumably include TRN terminals, another population of F1 profiles, most likely interneuron axons, provides input to GABAergic interneuron dendrites. Our results suggest that the TRN terminals are ideally situated to modulate thalamocortical transmission by controlling the response mode of thalamocortical cells. R. 1989. Intrinsic properties of nucleus reticularis thalami neurones of the rat studied in vitro. J Physiol (Lond) 416:111-122. Bal T, McCormick DA. 1993. Mechanisms of oscillatory activity in guineapig nucleus reticularis thalami in vitro: a mammalian pacemaker. J Physiol (Lond) 468:669 -691. Beaulieu C, Cynader M. 1992. Preferential innervation of immunoreactive choline acetyltransferase synapses on relay cells of the cat's lateral geniculate nucleus: a double-labeling study. Neuroscience 47:33-44. Benes FM, Lange N. 2001. Two-dimensional versus three-dimensional cell counting: a practical perspective. Trends Neurosci 24:11-17. Berman N. 1977. Connections of the pretectum in the cat. J Comp Neurol 174:227-254. Berson DM, Graybiel AM. 1978. Parallel thalamic zones in the LP-pulvinar complex of the cat identified by their afferent and efferent connections. Brain Res 147:139 -148. Berson DM, Graybiel AM. 1983. Organization of the striate-recipient zone of the cat's lateralis posterior-pulvinar complex and its relations with the geniculostriate system. Neuroscience 9:337-372. Bickford ME, Gunluk AE, Van Horn SC, Vaughan JW, Godwin DW, Sherman SM. 1994. Thalamic reticular nucleus synaptic targets in the cat LGN. Soc Neurosci Abstr 20:8. Bourassa J, Deschênes M. 1995. Corticothalamic projections from the primary visual cortex in rats: a single fiber study using biocytin as an anterograde tracer. Neuroscience 66:253-263. Carden WB, Bickford ME. 1999. Location of muscarinic type 2 receptors within the synaptic circuitry of the cat visual thalamus. J Comp Neurol 410:431-443. Coleman KA, Mitrofanis J. 1996. Organization of the visual reticular thalamic nucleus of the rat. Eur J Neurosci 8:388 -404. Conley M, Diamond IT. 1990. Organization of the visual sector of the thalamic reticular nucleus in Galago: evidence that the dorsal lateral geniculate and pulvinar nuclei occupy separate parallel tiers. Eur J Neurosci 2:211-226. Conley M, Kupersmith AC, Diamond IT. 1991. The organization of projections from subdivisions of the auditory cortex and thalamus to the auditory sector of the thalamic reticular nucleus in Galago. Eur J Neurosci 3:1089 -1103. Contreras D, Curro Dossi R, Steriade M. 1993. Electrophysiological properties of cat reticular thalamic neurones in vivo. J Physiol (Lond) 470:273-294. Crabtree JW. 1992. The somatotopic organization within the cat's thalamic reticular nucleus. Eur J Neurosci 4:1352-1361. Crabtree JW. 1996. Organization in the somatosensory sector of the cat's thalamic reticular nucleus. J Comp Neurol 366:207-222. Crabtree JW. 1998. Organization in the auditory sector of the cat's thalamic reticular nucleus. J Comp Neurol 390:167-182. Crabtree JW, Killackey HP. 1989. The topographic organization and axis of projection within the visual sector of the rabbit's thalamic reticular nucleus. Eur J Neurosci 1:94 -109. Cucchiaro JB, Uhlrich DJ, Sherman SM. 1991a. Electron-microscopic analysis of synaptic input from the perigeniculate nucleus to the A-laminae of the lateral geniculate nucleus in cats. J Comp Neurol 310:316 -336. Cucchiaro JB, Bickford ME, Sherman SM. 1991b. A GABAergic projection
A new interpretation of thalamocortical circuitry
Philosophical Transactions of the Royal Society B: Biological Sciences, 2002
Almost all the information that is needed to specify thalamocortical and neocortical wiring derives from patterned electrical activity induced by the environment. Wiring accuracy must be limited by the anatomical specificity of the cascade of events triggered by neural activity and culminating in synaptogenesis. We present a simple model of learning in the presence of plasticity errors. One way to achieve learning specificity is to build better synapses. We discuss an alternative, circuit–based, approach that only allows plasticity at connections that support highly selective correlations. This circuit resembles some of the more puzzling aspects of thalamocorticothalamic circuitry.