The effect of early sensory experience on development of neuron functional properties in the area of vibrissal projection in the rat neocortex

The role of specific sensory inflow in the functional maturation of neurons in the area of vibrissal projections in the somatosensory cortex of rats was studied. Animals were subjected to bilateral trimming of whiskers during the first three weeks of postnatal ontogenesis. Quantitative and qualitative characteristics of neuronal responses were analyzed in the "lemniscal" layers IV and Vb and "paralemniscal" layer Va in junior (27-40 PN days) and elder (41-57 PN days) rats. The immediate effect of deafferentation in younger animals consisted in an increase in excitatory responses, which correlated with a deficit of inhibitory reactions. In animals subjected to vibrissectomy, atypical responses were observed in the "lemniscal" and "paralemniscal" layers. This effect may be caused by a derangement of distribution of thalamic afferents in the somatosensory cortex. Elder animals in vibrissectomized group displayed an increase in inhibitory reactions, i.e., the long-term effect of vibrissectomy is the actualization of inhibitory mechanisms.     

Neuronal oscillations and multisensory interaction in primary auditory cortex

Recent anatomical, physiological, and neuroimaging findings indicate multisensory convergence at early, putatively unisensory stages of cortical processing. The objective of this study was to confirm somatosensory-auditory interaction in A1 and to define both its physiological mechanisms and its consequences for auditory information processing. Laminar current source density and multiunit activity sampled during multielectrode penetrations of primary auditory area A1 in awake macaques revealed clear somatosensory-auditory interactions, with a novel mechanism: somatosensory inputs appear to reset the phase of ongoing neuronal oscillations, so that accompanying auditory inputs arrive during an ideal, high-excitability phase, and produce amplified neuronal responses. In contrast, responses to auditory inputs arriving during the opposing low-excitability phase tend to be suppressed. Our findings underscore the instrumental role of neuronal oscillations in cortical operations. The timing and laminar profile of the multisensory interactions in A1 indicate that nonspecific thalamic systems may play a key role in the effect.     

Barrel cortex and whisker-mediated behaviors

Neural networks of the rodent barrel cortex are particularly tractable for developing a quantitative understanding of response transformations in a cortical column. A column in barrel cortex consists of approximately 10 compartments. Two thalamic input pathways, a sensory lemniscal one and sensorimotor paralemniscal one, are transformed to approximately 7 population outputs, each with distinct spatiotemporal response characteristics. Granular and supragranular layers are sites of segregated processing in lemniscal and paralemniscal pathways, whereas infragranular layers are sites of intracolumnar, lemniscal/paralemniscal integration. Individual thalamocortical connections are relatively weak, and a considerable fraction of thalamocortical afferents contributes to each sensory response. Intracortically, relatively few but strong synaptic connections contribute to sensory responses, and responses are rapidly terminated by inhibition. Overall cortical population activity is very low. Whiskers mediate a wide range of behaviors and many natural tactile behaviors occur very rapidly. Vibrissal object recognition can be size invariant and motion invariant and is based on the tactile 'Gestaltwahrnehmung' of shape.     

Spinal dorsal column afferent fiber composition in the pigeon: an electrophysiological investigation

Summary The spinal dorsal column of homing pigeons (Colomba livia) was investigated electrophysiologically by recording responses from individual afferent fibers at a high cervical level (segments C4-C5) to mechanical stimulation of wing skin and deep tissue. Of 157 afferent fibers 134 were cutaneous afferents. The remainder were afferents of deep receptors.Thirty of the cutaneous afferents were slowly adapting and 87 rapidly adapting (17 not identified). Rapidly adapting afferents were studied with regard to Pacinianlike characteristics (Herbst corpuscles in birds; vibration sensitive receptors). Of 43 rapidly adapting afferents 38 were classified as afferents of vibration sensitive Herbst corpuscles and 5 as non vibration sensitive rapidly adapting afferents; 44 afferents could not be studied sufficiently with regard to vibrational stimuli. The vibration sensitive Herbst corpuscle afferents had U-shaped vibrational tuning curves and responded best to vibration frequencies of 300 to 400 Hz. The 11 threshold for 300 Hz vibration ranged from 2 to 36 um. Herbst corpuscle afferents always showed strong phase coupling to the stimulus cycle.Afferents of deep receptors showed slowly adapting responses to firm pressure or movements of limbs and were classified as joint receptors. No muscle spindle afferents were encountered.Primary afferent fibers were identified in 89 cases (80 cutaneous and 9 deep), postsynaptic elements in 15 cases (11 cutaneous, 4 deep). Only slowly adapting responses were found in postsynaptic fibers.Abbreviations CV coefficient of variation - EI entrainment index - INTH interval histogram - PSTH peristimulus time histogram - RA rapidly adapting - SA slowly adapting     

Morphological changes of the terminations of afferent pathways in a neurodegenerative lesion induced by kainic acid

30 days after kainic acid injection into the rat ventrobasal thalamus, lemniscal afferents were labeled using wheat-germ agglutinin conjugated to HRP. They appeared considerably swollen in the area where neuronal post-synaptic targets had been eliminated. Electron microscopic analysis of the lesioned tissue revealed the presence of large profiles containing numerous organelles, particularly smooth endoplasmic reticulum, and giving rise to thin excrescences filled with neurofilaments. Since these morphological features are typical of regenerating "growth cones", we conclude that afferent terminals deprived of their post-synaptic targets undergo morphological changes preparing them for new synapses.     

Receptive field properties of near neighbor orientation selective neurons in the visual cortex: a modeling study

The primary visual cortex is organized into clusters of cells having similar receptive fields (RFs). A purely feedforward model has been shown to produce realistic simple cell receptive fields. The modeled cells capture a wide range of receptive field properties of orientation selective cortical cells. We have analyzed the responses of 78 nearby cell pairs to study which RF properties are clustered. Orientation preference shows strongest clustering. Orientation tuning width (hwhh) and tuning height (spikes/sec) at the preferred orientation are not as tightly clustered. Spatial frequency is also not as tightly clustered and RF phase has the least clustering. Clustering property of orientation preference, orientation tuning height and width depend on the location of cells in the orientation map. No such location dependence is observed for spatial frequency and RF phase. Our results agree well with experimental data.     

Effect of catecholaminergic transmission deficiency upon neuronal responses of the ventrolateral thalamic nucleus evoked by stimulation of cerebellar and pallidal inputs

During chronic experiments on cats, we investigated neuronal responses of the ventrolateral thalamic nucleus (VL) to stimulation of afferent inputs before and after injection of haloperidol and droperidol in cataleptic doses. In contrast to reactions in intact animals, the initial excitatory response of the VL neurons to stimulation of the cerebellar input after injection of neuroleptics was characterized by irregularity of manifestation and variability of the latent period; responses were in the form of burst discharges. Upon stimulation of pallidal afferents there was a consistent increase in the number of initial inhibitory responses consisting of two periods of suppression of background activity separated by an excitatory phase, at the same time that monophase inhibitory responses (68%) predominated in intact animals. Under neuroleptics, responses exhibiting a rhythmic alternation of periods of excitation and inhibition of impulse activity with a frequency of 3–5/sec appeared. It is proposed that these features of VL neuronal responses are a consequence of a hyperpolarized state of neurons caused by argumentation of external inhibitory influences in connection with blocking of the dopamine D2-receptors of the nigrostriatal system or due to a weakening of depolarizing influences during disruption of central -adrenergic transmission.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 23, No. 2, pp. 222–231, March–April, 1991.     

Modulation of the dynamics of cerebellar Purkinje cells through the interaction of excitatory and inhibitory feedforward pathways

The dynamics of cerebellar neuronal networks is controlled by the underlying building blocks of neurons and synapses between them. For which, the computation of Purkinje cells (PCs), the only output cells of the cerebellar cortex, is implemented through various types of neural pathways interactively routing excitation and inhibition converged to PCs. Such tuning of excitation and inhibition, coming from the gating of specific pathways as well as short-term plasticity (STP) of the synapses, plays a dominant role in controlling the PC dynamics in terms of firing rate and spike timing. PCs receive cascade feedforward inputs from two major neural pathways: the first one is the feedforward excitatory pathway from granule cells (GCs) to PCs; the second one is the feedforward inhibition pathway from GCs, via molecular layer interneurons (MLIs), to PCs. The GC-PC pathway, together with short-term dynamics of excitatory synapses, has been a focus over past decades, whereas recent experimental evidence shows that MLIs also greatly contribute to controlling PC activity. Therefore, it is expected that the diversity of excitation gated by STP of GC-PC synapses, modulated by strong inhibition from MLI-PC synapses, can promote the computation performed by PCs. However, it remains unclear how these two neural pathways are interacted to modulate PC dynamics. Here using a computational model of PC network installed with these two neural pathways, we addressed this question to investigate the change of PC firing dynamics at the level of single cell and network. We show that the nonlinear characteristics of excitatory STP dynamics can significantly modulate PC spiking dynamics mediated by inhibition. The changes in PC firing rate, firing phase, and temporal spike pattern, are strongly modulated by these two factors in different ways. MLIs mainly contribute to variable delays in the postsynaptic action potentials of PCs while modulated by excitation STP. Notably, the diversity of synchronization and pause response in the PC network is governed not only by the balance of excitation and inhibition, but also by the synaptic STP, depending on input burst patterns. Especially, the pause response shown in the PC network can only emerge with the interaction of both pathways. Together with other recent findings, our results show that the interaction of feedforward pathways of excitation and inhibition, incorporated with synaptic short-term dynamics, can dramatically regulate the PC activities that consequently change the network dynamics of the cerebellar circuit.     

Signal propagation in feedforward neuronal networks with unreliable synapses

In this paper, we systematically investigate both the synfire propagation and firing rate propagation in feedforward neuronal network coupled in an all-to-all fashion. In contrast to most earlier work, where only reliable synaptic connections are considered, we mainly examine the effects of unreliable synapses on both types of neural activity propagation in this work. We first study networks composed of purely excitatory neurons. Our results show that both the successful transmission probability and excitatory synaptic strength largely influence the propagation of these two types of neural activities, and better tuning of these synaptic parameters makes the considered network support stable signal propagation. It is also found that noise has significant but different impacts on these two types of propagation. The additive Gaussian white noise has the tendency to reduce the precision of the synfire activity, whereas noise with appropriate intensity can enhance the performance of firing rate propagation. Further simulations indicate that the propagation dynamics of the considered neuronal network is not simply determined by the average amount of received neurotransmitter for each neuron in a time instant, but also largely influenced by the stochastic effect of neurotransmitter release. Second, we compare our results with those obtained in corresponding feedforward neuronal networks connected with reliable synapses but in a random coupling fashion. We confirm that some differences can be observed in these two different feedforward neuronal network models. Finally, we study the signal propagation in feedforward neuronal networks consisting of both excitatory and inhibitory neurons, and demonstrate that inhibition also plays an important role in signal propagation in the considered networks.     

Robustness of neuronal tuning to binaural sound localization cues against age-related loss of inhibitory synaptic inputs

Sound localization relies on minute differences in the timing and intensity of sound arriving at both ears. Neurons of the lateral superior olive (LSO) in the brainstem process these interaural disparities by precisely detecting excitatory and inhibitory synaptic inputs. Aging generally induces selective loss of inhibitory synaptic transmission along the entire auditory pathways, including the reduction of inhibitory afferents to LSO. Electrophysiological recordings in animals, however, reported only minor functional changes in aged LSO. The perplexing discrepancy between anatomical and physiological observations suggests a role for activity-dependent plasticity that would help neurons retain their binaural tuning function despite loss of inhibitory inputs. To explore this hypothesis, we use a computational model of LSO to investigate mechanisms underlying the observed functional robustness against age-related loss of inhibitory inputs. The LSO model is an integrate-and-fire type enhanced with a small amount of low-voltage activated potassium conductance and driven with (in)homogeneous Poissonian inputs. Without synaptic input loss, model spike rates varied smoothly with interaural time and level differences, replicating empirical tuning properties of LSO. By reducing the number of inhibitory afferents to mimic age-related loss of inhibition, overall spike rates increased, which negatively impacted binaural tuning performance, measured as modulation depth and neuronal discriminability. To simulate a recovery process compensating for the loss of inhibitory fibers, the strength of remaining inhibitory inputs was increased. By this modification, effects of inhibition loss on binaural tuning were considerably weakened, leading to an improvement of functional performance. These neuron-level observations were further confirmed by population modeling, in which binaural tuning properties of multiple LSO neurons were varied according to empirical measurements. These results demonstrate the plausibility that homeostatic plasticity could effectively counteract known age-dependent loss of inhibitory fibers in LSO and suggest that behavioral degradation of sound localization might originate from changes occurring more centrally.     

CCK-induced inhibition of presympathetic vasomotor neurons: dependence on subdiaphragmatic vagal afferents and central NMDA receptors in the rat

Systemic administration of cholecystokinin (CCK) inhibits a subpopulation of rostral ventrolateral medulla (RVLM) presympathetic vasomotor neurons. This study was designed to determine whether this effect involved subdiaphragmatic vagal afferents and/or central N-methyl-d-aspartic acid (NMDA) receptors. Recordings were made from CCK-sensitive RVLM presympathetic vasomotor neurons in halothane-anesthetized, paralyzed male Sprague-Dawley rats. The responses of the neurons to CCK (2 and 4 microg/kg iv), phenylephrine (PE; 5 microg/kg iv), and phenylbiguanide (PBG; 5 microg/kg iv) were tested before and after application of the local anesthetic lidocaine (2% wt/vol gel; 1 ml) to the subdiaphragmatic vagi at the level of the esophagus. In seven separate experiments, lidocaine markedly reduced the inhibitory effects of CCK on RVLM presympathetic neuronal discharge rate. In other experiments, the effect of systemic administration of dizocilpine (1 mg/kg iv), a noncompetitive antagonist at NMDA receptor ion channels, on the RVLM presympathetic neuronal responses to CCK, PBG, and PE was tested. In all cases (n = 6 neurons in 6 individual rats), dizocilpine inhibited the effects of CCK, PBG, and PE on RVLM presympathetic neuronal discharge. These results suggest that the effects of systemic CCK on the discharge of RVLM presympathetic neurons is mediated via an action on receptors located on subdiaphragmatic vagal afferents. Furthermore, the data suggest that CCK activates a central pathway involving NMDA receptors to produce inhibition of RVLM presympathetic neuronal discharge.     

Spatio-temporal convergence (STC) in otolith neurons

It has been recently demonstrated that some primary otolith afferents and most otolith-related vestibular nuclei neurons encode two spatial dimensions that can be described by two vectors in temporal and spatial quadrature. These cells are called broadly-tuned neurons. They are characterized by a non-zero tuning ratio which is defined as the ratio of the minimum over the maximum sensitivity of the neuron. Broadly-tuned neurons exhibit response gains that do not vary according to the cosine of the angle between the stimulus direction and the cell's maximum sensitivity vector and response phase values that depend on stimulus orientation. These responses were observed during stimulation with pure linear acceleration and can be explained by spatio-temporal convergence (STC) of primary otolith afferents and/or otolith hair cells. Simulations of STC of the inputs to primary otolith afferents and vestibular nuclei neurons have revealed interesting characteristics: First, in the case of two narrowly-tuned input signals, the largest tuning ratio is achieved when the input signals are of equal gain. The smaller the phase difference between the input vectors, the larger the orientation differences that are required to produce a certain tuning ratio. Orientation and temporal phase differences of 30–40° create tuning ratios of approximately 0.10–0.15 in target neurons. Second, in the case of multiple input signals, the larger the number of converging inputs, the smaller the tuning ratio of the target neuron. The tuning ratio depends on the number of input units, as long as there are not more than about 10. For more than 10–20 input vectors, the tuning ratio becomes almost independent of the number of inputs. Further, if the inputs comprise two populations (with different gain and phase values at a given stimulus frequency), the largest tuning ratio is obtained when the larger population has a smaller gain. These findings are discussed in the context of known anatomical and physiological characteristics of innervation patterns of primary otolith afferents and their possible convergence onto vestibular nuclei neurons.     

Altered excitability of and synaptic effects of motoneurons during the establishing of a locomotor generation in the cat

Research was performed on spinal cats injected with DOPA and decorticate (decerebrated at level A 13) and spinal cats. It was found that formation (activation) of the spinal locomotor generator is accompanied by heightened excitability in the extensor and the reverse trend in the flexor motoneurons, by an increase in the efficacy of recurrent and reciprocal Ia inhibition of -motoneurons, and by a weakening of the influence of Ib afferents and extensor reflex afferents on these same motoneurons. The likely functional role of these changes in tuning of the spinal segmental apparatus in the generation of locomotor rhythm is discussed.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 18, No. 5, pp. 679–687, September–October, 1986.     

蛙下丘频率调谐特性方向选择性的建模和仿真

基于Ｆｅｎｇ等人的神经电生理实验结果,建立了关于豹蛙（Ｒａｎａ ｐｉｐｉｅｎ）半规隆凸（ｔｏｒｕｓ ｓｅｍｉｃｉｒｃｕｌａｒｉｓ）核团神经元频率调谐特性方向选择性反应的模型,并在此基础上讨论了模型各个参数对模型方向性反应输出的影响。结果提示：１）听觉系统两侧的相互抑制作用－双耳抑制主要决定频率调谐特性的尖锐性随方向变化的特性;２）前级神经元对不同方位外界声源刺激具有不同强度平均脉冲发放的特征则主要     

Lateral sharpening of cortical frequency tuning by approximately balanced inhibition

Cortical inhibition plays an important role in shaping neuronal processing. The underlying synaptic mechanisms remain controversial. Here, in vivo whole-cell recordings from neurons in the rat primary auditory cortex revealed that the frequency tuning curve of inhibitory input was broader than that of excitatory input. This results in relatively stronger inhibition in frequency domains flanking the preferred frequencies of the cell and a significant sharpening of the frequency tuning of membrane responses. The less selective inhibition can be attributed to a broader bandwidth and lower threshold of spike tonal receptive field of fast-spike inhibitory neurons than nearby excitatory neurons, although both types of neurons receive similar ranges of excitatory input and are organized into the same tonotopic map. Thus, the balance between excitation and inhibition is only approximate, and intracortical inhibition with high sensitivity and low selectivity can laterally sharpen the frequency tuning of neurons, ensuring their highly selective representation.     

Large-scale modeling of the primary visual cortex: influence of cortical architecture upon neuronal response.

A large-scale computational model of a local patch of input layer 4 [Formula: see text] of the primary visual cortex (V1) of the macaque monkey, together with a coarse-grained reduction of the model, are used to understand potential effects of cortical architecture upon neuronal performance. Both the large-scale point neuron model and its asymptotic reduction are described. The work focuses upon orientation preference and selectivity, and upon the spatial distribution of neuronal responses across the cortical layer. Emphasis is given to the role of cortical architecture (the geometry of synaptic connectivity, of the ordered and disordered structure of input feature maps, and of their interplay) as mechanisms underlying cortical responses within the model. Specifically: (i) Distinct characteristics of model neuronal responses (firing rates and orientation selectivity) as they depend upon the neuron's location within the cortical layer relative to the pinwheel centers of the map of orientation preference; (ii) A time independent (DC) elevation in cortico-cortical conductances within the model, in contrast to a "push-pull" antagonism between excitation and inhibition; (iii) The use of asymptotic analysis to unveil mechanisms which underly these performances of the model; (iv) A discussion of emerging experimental data. The work illustrates that large-scale scientific computation--coupled together with analytical reduction, mathematical analysis, and experimental data, can provide significant understanding and intuition about the possible mechanisms of cortical response. It also illustrates that the idealization which is a necessary part of theoretical modeling can outline in sharp relief the consequences of differing alternative interpretations and mechanisms--with final arbiter being a body of experimental evidence whose measurements address the consequences of these analyses.     

A species-specific frequency filter through specific inhibition, not specific excitation

Many bushcrickets produce specific song spectra for acoustic communication. Song detection and/ or recognition may make use of such specificity. Where in the nervous system are the filters for song frequency situated? A peripheral tuning for song frequency typically does not exist. Auditory receptor cells of bushcrickets connect to local and ascending neurons in the prothoracic ganglion. One of the ascending neurons (1) may function as a frequency filter in a group of four related bushcrickets (genera Ancistrura, Barbitistes). The frequency response of ascending neuron 1 is species-specific roughly corresponding to the frequency of the conspecific male song. The species-specific tuning of the neuron is not brought about by specific excitation, but by specific inhibition. By eliminating this frequency-dependent and species-specific inhibition the former filter neuron is transformed into an unspecific broad-band neuron in all four species. Its tuning then does not differ from omega neuron 1, a local neuron which is rather unspecific for frequency. Also, the supra-threshold responses of ascending neuron 1, which are different in intact animals, are similar to each other and similar to omega neuron 1 following elimination of inhibition. Only ascending neuron 1 of Ancistrura retains some species-specific features at low frequencies. In conclusion, evolution changed inhibition, not excitation of a species-specific neuron.     

Reflex mechanisms of fore-hindlimb relations demonstrable in lumbar flexor centers of the cat spinal cord

The dynamics of interaction between segmental, propriospinal, and spino-bulbo-spinal components of reflex responses of lumbar flexor centers was investigated during activation of forelimb and hindlimb afferents in cats. The monosynaptic flexor reflex to activation of hindlimb afferents is facilitated up to 300% when it coincides in time with the reflex discharge evoked by activation of forelimb afferents, and it remains increased up to 120–140% for 40–50 msec during the aftereffect of such activation. Polysynaptic flexor reflexes of segmental, propriospinal, and spino-bulbo-spinal origin have both facilitatory and inhibitory effects on each other. Facilitation is observed only while the interacting responses coincide in time, inhibition when they do not coincide. Three type of inhibitory effects with durations of 7–15, 40–150, and 300–500 msec are observed. The possible neuronal mechanisms of interaction between these reflexes and their role in functional relations between the fore- and hindlimbs are discussed.     

Thalamocortical control of feed-forward inhibition in awake somatosensory 'barrel' cortex

Intracortical inhibition plays a role in shaping sensory cortical receptive fields and is mediated by both feed-forward and feedback mechanisms. Feed-forward inhibition is the faster of the two processes, being generated by inhibitory interneurons driven by monosynaptic thalamocortical (TC) input. In principle, feed-forward inhibition can prevent targeted cortical neurons from ever reaching threshold when TC input is weak. To do so, however, inhibitory interneurons must respond to TC input at low thresholds and generate spikes very quickly. A powerful feed-forward inhibition would sharpen the tuning characteristics of targeted cortical neurons, and interneurons with sensitive and broadly tuned receptive fields could mediate this process. Suspected inhibitory interneurons (SINs) with precisely these properties are found in layer 4 of the somatosensory (S1) 'barrel' cortex of rodents and rabbits. These interneurons lack the directional selectivity seen in most cortical spiny neurons and in ventrobasal TC afferents, but are much more sensitive than cortical spiny neurons to low-amplitude whisker displacements. This paper is concerned with the activation of S1 SINs by TC impulses, and with the consequences of this activation. Multiple TC neurons and multiple S1 SINs were simultaneously studied in awake rabbits, and cross-correlation methods were used to examine functional connectivity. The results demonstrate a potent, temporally precise, dynamic and highly convergent/divergent functional input from ventrobasal TC neurons to SINs of the topographically aligned S1 barrel. Whereas the extensive pooling of convergent TC inputs onto SINs generates sensitive and broadly tuned inhibitory receptive fields, the potent TC divergence onto many SINs generates sharply synchronous activity among these elements. This TC feed-forward inhibitory network is well suited to provide a fast, potent, sensitive and broadly tuned inhibition of targeted spiny neurons that will suppress spike generation following all but the most optimal feed-forward excitatory inputs.     

Timing and specificity of feed-forward inhibition within the LGN

Local interneurons provide feed-forward inhibition from retinal ganglion cells (RGCs) to thalamocortical (TC) neurons, but questions remain regarding the timing, magnitude, and functions of this inhibition. Here, we identify two types of inhibition that are suited to play distinctive roles. We recorded excitatory and inhibitory postsynaptic currents (EPSCs/IPSCs) in TC neurons in mouse brain slices and activated individual RGC inputs. In 34% of TC neurons, we identified EPSCs and IPSCs with identical thresholds that were tightly correlated, indicating activation by the same RGC. Such "locked" IPSCs occurred 1 ms after EPSC onset. The remaining neurons had only "nonlocked" inhibition, in which EPSCs and IPSCs had different thresholds, indicating activation by different RGCs. Nonlocked inhibition may refine receptive fields within the LGN by providing surround inhibition. In contrast, dynamic-clamp recordings suggest that locked inhibition improves the precision of synaptically evoked responses in individual TC neurons by eliminating secondary spikes.