Efficacy of thalamocortical and intracortical synaptic connections: quanta, innervation, and reliability (original) (raw)

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-