Journal of Neurophysiology

Surmeier, D. J.; Towe, A. L.

doi: N/Apmid: 3585465

Abstract The intrinsic processes contributing to the three discharge patterns of proprioceptive cuneate neurons described by Surmeier and Towe were studied experimentally and with computer simulation. Examination of the alterations in excitability produced by antidromic activation suggested that a prolonged inhibition was a concomitant of discharge in proprioceptive cuneate neurons. Computer simulation was performed to test the possible roles of inhibitory hyperpolarizing processes in governing the observed discharge patterns. These simulations used two constant threshold models. The simplest model linearly integrated synaptic potentials until the spike threshold was reached. After the discharge, synaptic potentials that preceded the spike were ignored (i.e., the model was "reset"). The second model was similar to the first except that following a spike two hyperpolarizing processes were activated and preceding events continued to play a role in membrane potential. Simulation of class A spike trains that possessed positive correlations between nearby intervals was successful only with a resetting model. This suggested that class A neurons have fast, no-memory postspike conductance changes, which effectively shunt synaptic charge. Simulation of class B spike trains was possible with the nonresetting model. At least two periodic inputs, which evoked brief, relatively large EPSPs, were required. In addition, a prominent, fast, spike-dependent hyperpolarization and a small-amplitude, slow hyperpolarization were required. Simulation of class C spike trains was also possible with the nonresetting model. Several periodic inputs were required; one input had to evoke a slow suprathreshold EPSP. In contrast to class B simulations, class C spike train simulation required that a large-amplitude, slow hyperpolarization, as well as a brief hyperpolarization, following spike initiation. The results of class B and C simulations suggested that these two groups differed primarily in the amplitude of a slow, hyperpolarizing, postspike conductance. Some role may also be played by the time course of the driving EPSPs. Copyright © 1987 the American Physiological Society

Surmeier, D. J.; Towe, A. L.

doi: N/Apmid: 3585464

Abstract Fifty-two slowly adapting proprioceptive neurons in the cuneate nucleus of chloralose-anesthetized cats were studied. Recordings were made from 3 mm rostral to the obex to 5 mm caudal. The highest densities of proprioceptive neurons were found above and more than 3 mm caudal to the obex. Analysis of the spike trains produced with the forelimb held fixed revealed three basic periodic patterns. Neurons exhibiting these patterns were partitioned into three groups, referred to as the A, B, and C classes. Class A neurons (42%; 22/52) produced regular spike trains that were qualitatively similar to muscle spindle fibers. Interval distributions for this class were typically unimodal and slightly positively skewed. Adjacent intervals were frequently positively correlated. Spectral analysis suggested that 91% of class A spike trains had one to two periodic components. Class B neurons (21%; 11/52) had additional spikes interposed in their periodic discharge; these "interrupting" spikes did not significantly alter the timing of the dominant periodic discharge. Interval distributions were typically bimodal and adjacent intervals were negatively correlated. Spectral analysis suggested that two or more periodic components were present in their spike trains. Class C neurons (36%; 26/52) had spike trains with a basic rhymicity, but when this specific discharge was interrupted, the subsequent interval was near modal length; thus, they were "reset." Interval distributions were usually multimodal and adjacent intervals were frequently negatively correlated. Spectral analysis suggested that C spike trains usually had four or more periodic components. Estimates of information-carrying capacity of each class using a mean rate code and those of primary muscle spindle fibers suggested that a sizable information loss may occur in synaptic transmission. This potential loss was smaller for A-neurons (40%) than for B- (69%) or C-neurons (64%). Electrical stimulation of cutaneous structures influenced 55% (22/52) of the sample. All were members of the B and C classes. Responses were typically biphasic. The cutaneous receptive fields nearly always included a portion of the forepaw. No relationship was found between movement sensitivity and receptive field topography. Contralateral input was found in half (10/20) the neurons tested. Copyright © 1987 the American Physiological Society

Gillespie, M. J.; Gordon, T.; Murphy, P. R.

doi: N/Apmid: 2953872

Abstract A reexamination of the question of specificity of reinnervation of fast and slow muscle was undertaken using the original "self" nerve supply to the fast lateral gastrocnemius (LG) and slow soleus muscles in the rat hindlimb. This paradigm takes advantage of the unusual situation of a common nerve branch, which supplies both a fast and slow muscle, and of the opportunity to keep the reinnervating nerve in its normal position. In addition it provides a test of the effects of cross-reinnervation among muscles of the same functional group. The properties of soleus and LG muscles and of individual muscle units were characterized in normal rats and in rats 4-14 mo after cutting the lateral gastrocnemius-soleus (LGS) nerve and suture of the proximal stump to the dorsal surface of the LG muscle. Individual muscle units were functionally isolated by stimulation of single motor axons to LG or soleus muscle contained in teased filaments in the L4 and L5 ventral roots. Motor units were classified as fast contracting fatiguable (FF), fast contracting fatigue resistant (FR), and slow (S) on the basis of criteria described in the cat by Burke et al. and applied to rat muscle units by Gillespie et al. Muscle fibers were classified as fast glycolytic (FG), fast oxidative glycolytic (FOG), and slow oxidative (SO) on the basis of histochemical staining for myosin ATPase, nicotinamide-adenine dinucleotide diaphorase (NADH-D), and alpha-glycerophosphate (alpha-GPD). Reinnervated muscles developed less force and weighed less in accordance with having fewer than normal motor units and having lost denervated muscle fibers. Normal LG contained a small proportion of S-type motor units (9%), whereas the majority (80%) of control soleus units were S type. After reinnervation, each muscle contained similar proportions of fast and slow motor units with S-type units constituting 30% of units in both muscles. When compared with the normal motor-unit sample, there was no significant change in average twitch and tetanic force in reinnervated muscles for each type of motor unit. However, the range within each type was greater, and there was considerable overlap between types. Twitch contraction time was inversely correlated with force in normal and reinnervated muscles as shown previously in self- and cross-reinnervated LGS in the cat. Changes in proportions of motor units in reinnervated LG were accompanied by corresponding changes in histochemical muscle types. This contrasted with reinnervated soleus in which the proportion of muscle fiber types was not significantly changed from normal despite significant change in motor-unit proportions.(ABSTRACT TRUNCATED AT 400 WORDS) Copyright © 1987 the American Physiological Society

Winslow, R. L.; Sachs, M. B.

doi: N/Apmid: 3585452

Abstract The discharge rates of single auditory-nerve fibers responding to best-frequency (BF) tones of varying level presented simultaneously with fixed level broadband noise were recorded with and without electrical stimulation of the crossed olivocochlear bundle (COCB). In the absence of COCB stimulation, monotonic increases in noise level produce monotonic increases in the low-level noise-driven response rate of auditory nerve fibers. As a result of adaptation, these increases in noise-driven response rate produce monotonic decreases in saturation discharge rate. At high noise levels, these compressive effects may eliminate the differential rate response of auditory nerve fibers to BF tones. COCB stimulation can restore this differential rate response by producing large decreases in noise-driven response rate and large increases in saturation discharge rate. In backgrounds of quiet, COCB stimulation is known to shift the dynamic range of single auditory nerve fiber BF tone responses to higher stimulus levels. In the presence of background noise, COCB stimulation produces upward shift of dynamic range, which decreases with increasing noise level. At high noise levels, COCB-induced decompression of rate-level functions may occur with little or no dynamic range shift. This enables auditory nerve fibers to signal changes in tone level with changes in discharge rate at lower signal-to-noise ratios than would be possible otherwise. Broadband noise also produces upward shift of the dynamic range of single auditory nerve fiber BF tone response. Noise-induced dynamic range shift of BF tone response was measured as a function of noise level with and without COCB stimulation. COCB stimulation elevates the threshold of noise-induced dynamic range shift. This shift is thought to result from two-tone rate suppression. Increases in the threshold of noise-induced shift due to COCB stimulation therefore suggests an interaction between the mechanism of two-tone rate suppression and the mechanism by which COCB stimulation produces dynamic range shift. These interactions were further investigated by recording auditory nerve fiber rate responses to fixed-level BF excitor tones presented simultaneously with fixed-frequency variable level suppressor tones. Rate responses were recorded with and without COCB stimulation. Experimental results were quantified using a phenomenological model of two-tone rate suppression presented by Sachs and Abbas. Copyright © 1987 the American Physiological Society

Schiller, P. H.; Sandell, J. H.; Maunsell, J. H.

doi: N/Apmid: 3585453

Abstract Rhesus monkeys were trained to make saccadic eye movements to visual targets using detection and discrimination paradigms in which they were required to make a saccade either to a solitary stimulus (detection) or to that same stimulus when it appeared simultaneously with several other stimuli (discrimination). The detection paradigm yielded a bimodal distribution of saccadic latencies with the faster mode peaking around 100 ms (express saccades); the introduction of a pause between the termination of the fixation spot and the onset of the target (gap) increased the frequency of express saccades. The discrimination paradigm, on the other hand, yielded only a unimodal distribution of latencies even when a gap was introduced, and there was no evidence for short-latency "express" saccades. In three monkeys either the frontal eye field or the superior colliculus was ablated unilaterally. Frontal eye field ablation had no discernible long-term effects on the distribution of saccadic latencies in either the detection or discrimination tasks. After unilateral collicular ablation, on the other hand, express saccades obtained in the detection paradigm were eliminated for eye movements contralateral to the lesion, leaving only a unimodal distribution of latencies. This deficit persisted throughout testing, which in one monkey continued for 9 mo. Express saccades were not observed again for saccades contralateral to the lesion, and the mean latency of the contralateral saccades was longer than the mean latency of the second peak for the ipsiversive saccades. The latency distribution of saccades ipsiversive to the collicular lesion was unaffected except for a few days after surgery, during which time an increase in the proportion of express saccades was evident. Saccades obtained with the discrimination paradigm yielded a small but reliable increase in saccadic latencies following collicular lesions, without altering the shape of the distribution. Unilateral muscimol injections into the superior colliculus produced results similar to those obtained immediately after collicular lesions: saccades contralateral to the injection site were strongly inhibited and showed increased saccadic latencies. This was accompanied by a decrease of ipsilateral saccadic latencies and an increase in the number of saccades falling into the express range. The results suggest that the superior colliculus is essential for the generation of short-latency (express) saccades and that the frontal eye fields do not play a significant role in shaping the distribution of saccadic latencies in the paradigms used in this study.(ABSTRACT TRUNCATED AT 400 WORDS) Copyright © 1987 the American Physiological Society

Fukuda, M.; Ono, T.; Nakamura, K.

doi: N/Apmid: 3585454

Abstract Neural activity in either the amygdala (AM) or lateral hypothalamus (LHA) was examined while monkeys obtained food as a reward for operant bar pressing. Neurons in the AM were tested before, during, and after reversible cooling of the inferotemporal cortex (ITCx). LHA neurons were tested similarly except that the cooling probe was located in the AM. Cooling probes were chronically implanted bilaterally over the dura of the anterior ITCx in one monkey and in the lateral part of the AM in two monkeys. The activity of 43 AM neurons was analyzed. Before ITCx cooling, each AM neuron was classified into one of four groups based on its response pattern: 6 neurons responded primarily to the sight of food, 11 responded primarily to the sight of nonfood objects, 21 responded to the sight of both food and nonfood (arousal related), and 5 neurons did not respond. ITCx cooling changed the spontaneous firing rate of 15 AM neurons (2 increased, 13 decreased). Responses to the sight of food and/or nonfood of two food-related, four nonfood-related, and seven arousal-related neurons were depressed, and responses of two nonfood-related and three arousal-related neurons were enhanced. Of 17 neurons that were normally food or nonfood specific, 8 became nondiscriminative during ITCx cooling. The activity of 55 LHA neurons was tested. Of these, 22 were food related, 6 responded primarily during ingestion, 22 were arousal related, and 5 did not respond. AM cooling changed the spontaneous firing rates of 21 LHA neurons (12 increased, 9 decreased). Visual responses of nine food-related neurons and two arousal-related neurons were depressed by AM cooling. Ingestion-related responses in the AM (3 of 6 food-related neurons) were not affected by ITCx cooling, but responses of three ingestion-related LHA neurons (3/6) were depressed by AM cooling. The data suggest that dynamic interactions among the ITCx, the AM, and the LHA are important in discriminating between food and nonfood, and, consequently, in the stimulus-reinforcement process, i.e., recognition of reward or no reward. The results are discussed in terms of known anatomical data and behavioral evidence from earlier lesion experiments. Copyright © 1987 the American Physiological Society

Aitkin, L. M.; Martin, R. L.

doi: N/Apmid: 3585459

Abstract The responses to changes in stimulus azimuth of 220 high best-frequency (BF) (greater than 3 kHz) units in the central nucleus of the inferior colliculus of the anesthetized cat were studied with BF tones (220 units) and noise stimuli (84 units). By this means we hoped to gain some insights into the way the azimuthal locations of high BF stimuli were represented in the inferior colliculus. For each unit the discharge rate was determined for stimuli located along a plane tilted at 20 degrees above the horizontal. This plane was chosen to optimize pinna directionality. Locations in the frontal field were sampled in 10-20 degree steps around a 170 degree arc. These measurements were repeated at a number of different stimulus intensities until the directional properties of the unit became clear. Units for which the functions relating discharge rate to azimuth for a given stimulus showed a clear feature (peak or border), the azimuthal location of which varied little with intensities between 20 and 40 dB above threshold, were defined as being azimuth selective for that stimulus. Only 13% of units were azimuth selective for BF tones, whereas 44% were selective for noise. Many azimuth functions for selective units were of the plateau-shaped type for which relatively high discharge rates occurring at most contralateral azimuths declined steeply to near zero and remained low for most ipsilateral azimuths. These plateau-shaped functions were most common for tonal stimuli. Other functions showed a fixed azimuth of maximum firing (best azimuth); these were more common for noise than for tonal stimuli. Detailed azimuth functions for both tone and noise stimuli were measured for 63 units. Some exhibited the same kind of azimuth function to both stimuli. However, 18 units were azimuth selective to noise but not to tones. The borders of plateau-shaped functions obtained using both noise and tonal stimuli were concentrated within 20 degrees of the median plane. Very few units had borders that spanned peripheral ipsilateral or contralateral azimuths. Although the best azimuths of some noise azimuth functions were observed to lie at these peripheral azimuths, the majority occurred around 20 degrees contralateral to the median plane. The recording sites for units were related to a three-by-three matrix of rostrocaudal and mediolateral locations across the central nucleus. Units that were azimuth selective to noise were distributed fairly evenly throughout the central nucleus, whereas units azimuth selective to tones formed highest proportions rostrally.(ABSTRACT TRUNCATED AT 400 WORDS) Copyright © 1987 the American Physiological Society

Perlman, I.; Normann, R. A.; Anderton, P. J.

doi: N/Apmid: 2884281

Abstract The effects of prolonged superfusions with acidic amino acids and their agonists, kainic acid (KA) and N-methyl-D-aspartate (NMDA), on horizontal cells, and extracellular field potentials were studied in the turtle everted eyecup preparation using simultaneous intracellular and extracellular recordings. In a fresh preparation initial superfusions with each of the above agents usually induced a large (up to 60 mV) transient negative extracellular field potential recorded adjacent to horizontal cells, followed by a sustained negative potential of lesser amplitude (up to 10 mV). The amplitude of the sustained potential did not vary with subsequent superfusions, whereas that of the transient phase was reduced. KA and NMDA were much more potent (at least 300 times) in evoking these field potentials than either acidic amino acid. The horizontal cell transmembrane potential was monitored as the difference between the intra- and extracellular potentials. Superfusion with KA and NMDA produced a triphasic time course of the drug effect consisting of an initial depolarization with reduced photoresponses, a rehyperpolarization of the membrane accompanied by a growth of the light responses followed by a gradual depolarization and loss of photoresponses. Superfusion with the acidic amino acids usually produced a biphasic response that resembled qualitatively the first two phases of the response to KA and NMDA. This biphasic response was occasionally followed by a gradual depolarization and loss of the light response. The kinetics of the transient component of the field potential and the rapid reduction and regrowth of the photoresponses recorded during superfusion with these agents suggests an initial action of these drugs, which is of a nonsynaptic origin and which may be an expression of a drug-induced spreading depression. The kinetics of the photoresponses recorded during superfusion with KA, L-aspartate, and L-glutamate were similar but differed from those recorded during superfusion with NMDA. The difference in the effects of NMDA and KA on photoresponse kinetics suggests that two types of acidic amino acid receptors may be present in the outer plexiform layer of the turtle retina. Copyright © 1987 the American Physiological Society

Morales, F. R.; Engelhardt, J. K.; Soja, P. J.; Pereda, A. E.; Chase, M. H.

doi: N/Apmid: 3585456

Abstract It is well established that cholinergic agonists, when injected into the pontine reticular formation in cats, produce a generalized suppression of motor activity (1, 3, 6, 14, 18, 27, 33, 50). The responsible neuronal mechanisms were explored by measuring ventral root activity, the amplitude of the Ia-monosynaptic reflex, and the basic electrophysiological properties of hindlimb motoneurons before and after carbachol was microinjected into the pontine reticular formation of decerebrate cats. Intrapontine microinjections of carbachol (0.25-1.0 microliter, 16 mg/ml) resulted in the tonic suppression of ventral root activity and a decrease in the amplitude of the Ia-monosynaptic reflex. An analysis of intracellular records from lumbar motoneurons during the suppression of motor activity induced by carbachol revealed a considerable decrease in input resistance and membrane time constant as well as a reduction in motoneuron excitability, as evidenced by a nearly twofold increase in rheobase. Discrete inhibitory postsynaptic potentials were also observed following carbachol administration. The changes in motoneuron properties (rheobase, input resistance, and membrane time constant), as well as the development of discrete inhibitory postsynaptic potentials, indicate that spinal cord motoneurons were postsynaptically inhibited following the pontine administration of carbachol. In addition, the inhibitory processes that arose after carbachol administration in the decerebrate cat were remarkably similar to those that are present during active sleep in the chronic cat. These findings suggest that the microinjection of carbachol into the pontine reticular formation activates the same brain stem-spinal cord system that is responsible for the postsynaptic inhibition of alpha-motoneurons that occurs during active sleep. Copyright © 1987 the American Physiological Society

Swadlow, H. A.; Weyand, T. G.

doi: N/Apmid: 3585466

Abstract The intrinsic stability of the rabbit eye was exploited to enable receptive-field analysis of antidromically identified corticotectal (CT) neurons (n = 101) and corticogeniculate (CG) neurons (n = 124) in visual area I of awake rabbits. Eye position was monitored to within 1/5 degrees. We also studied the receptive-field properties of neurons synaptically activated via electrical stimulation of the dorsal lateral geniculate nucleus (LGNd). Whereas most CT neurons had either complex (59%) or motion/uniform (15%) receptive fields, we also found CT neurons with simple (9%) and concentric (4%) receptive fields. Most complex CT cells were broadly tuned to both stimulus orientation and velocity, but only 41% of these cells were directionally selective. We could elicit no visual responses from 6% of CT cells, and these cells had significantly lower conduction velocities than visually responsive CT cells. The median spontaneous firing rates for all classes of CT neurons were 4-8 spikes/s. CG neurons had primarily simple (60%) and concentric (9%) receptive fields, and none of these cells had complex receptive fields. CG simple cells were more narrowly tuned to both stimulus orientation and velocity than were complex CT cells, and most (85%) were directionally selective. Axonal conduction velocities of CG neurons (mean = 1.2 m/s) were much lower than those of CT neurons (mean = 6.4 m/s), and CG neurons that were visually unresponsive (23%) had lower axonal conduction velocities than did visually responsive CG neurons. Some visually unresponsive CG neurons (14%) responded with saccadic eye movements. The median spontaneous firing rates for all classes of CG neurons were less than 1 spike/s. All neurons synaptically activated via LGNd stimulation at latencies of less than 2.0 ms had receptive fields that were not orientation selective (89% motion/uniform, 11% concentric), whereas most cells with orientation-selective receptive fields had considerably longer synaptic latencies. Most short-latency motion/uniform neurons responded to electrical stimulation of the LGNd (and visual area II) with a high-frequency burst (500-900 Hz) of three or more spikes. Action potentials of these neurons were of short duration, thresholds of synaptic activation were low, and spontaneous firing rates were the highest seen in rabbit visual cortex. These properties are similar to those reported for interneurons in several regions in mammalian central nervous system. Nonvisual sensory stimuli that resulted in electroencephalographic arousal (hippocampal theta activity) had a profound effect on the visual responses of many visual cortical neurons.(ABSTRACT TRUNCATED AT 400 WORDS) Copyright © 1987 the American Physiological Society