Journal of Neurophysiology

Conway, J. L.; Schiller, P. H.

doi: N/Apmid: 6663330

Abstract This study investigated the organization of the dorsal lateral geniculate nucleus (LGN) of the tree shrew (Tupaia glis) using both microelectrode recording and anatomical techniques. The tree shrew LGN contains approximately 100,000 cells, of which 20% are in layers 2 and 6. These two layers receive input from the ipsilateral eye. The topography of the tree shrew LGN was delineated by taking systematic penetrations through the structure. Examination of the organization of the LGN laminae showed the following: in layer 1 (the lamina next to the optic tract) a mixture of on-center, off-center and on-off center cells was found; the majority of these cells responded transiently to visual stimuli and they had slightly longer conduction latencies than did cells in the other laminae. On-center and off-center cells in laminae 2-6 were sharply segregated: layers 2, 3, and 4 contained off-center cells and layers 5 and 6 contained on-center cells. Most of the cells in laminae 2-6 responded in a sustained manner to visual stimuli. These results suggest that one function of the LGN lamina is to group cells into various classes. Such grouping has now been shown to occur partially or completely for 1) eye of origin, 2) cell types characterized as on-center and off-center, and 3) cell types characterized as producing transient and sustained responses. The nature and degree of laminar specificity, however, varies considerably from species to species. Copyright © 1983 the American Physiological Society

Siegler, M. V.; Burrows, M.

doi: N/Apmid: 6663326

Abstract A population of spiking local interneurons in the metathoracic ganglion of the locust is vigorously excited by particular sensory stimuli from the hindlegs and participates in local postural reflexes. We examined the inputs from singly innervated mechanoreceptors (hairs and campaniform sensilla) to these spiking local interneurons, to nonspiking local interneurons, and to motor neurons that are also elements of local reflex pathways. Recordings were made intracellularly from the interneurons and motor neurons and extracellularly from afferent fibers. The physiological evidence is consistent with the spiking local interneurons being excited by direct, chemically mediated synaptic inputs from the afferents. Each afferent spike is followed at a constant latency by an excitatory postsynaptic potential (EPSP) in a spiking local interneuron, even at instantaneous frequencies as high as 300 Hz. The estimated synaptic delay is 1.5 ms, similar to that measured at other presumed monosynaptic connections within the same ganglion. Cobalt stains of individual interneurons, and of the central projections of afferent fibers show that both branch within the same ventral region of neuropil. Afferents from several hairs and campaniform sensilla converge on an individual spiking local interneuron. One interneuron is shown to receive inputs from at least seven hairs and four campaniform sensilla, but these represent only a tiny fraction of the total number of such sensilla on a hindleg. Practical limitations to the number of sensilla that can be tested for each interneuron means that the degree of convergence is likely to be considerably underestimated. We found no evidence that nonspiking local interneurons or motor neurons receive direct inputs from the afferents tested. Neurons of both types are, however, affected by stimulation of individual hairs, and the resulting pattern of postsynaptic potentials (PSPs) is similar to the pattern of spikes evoked in the spiking local interneurons. We infer from the evidence presented here and elsewhere (10, 11) that the spiking local interneurons are involved in at least two types of pathways for local interactions: 1) sensory neuron-spiking local interneuron-motor neuron, and 2) sensory neuron-spiking local interneuron-nonspiking local interneuron-motor neuron. We conclude that the spiking local interneurons are major elements in the primary integration of inputs from external receptors on the hindlegs. Copyright © 1983 the American Physiological Society

Walters, E. T.; Byrne, J. H.; Carew, T. J.; Kandel, E. R.

doi: N/Apmid: N/A

Abstract The tail-withdrawal reflex of Aplysia can be sensitized by weak stimulation of a site outside the site used to test the reflex or by repeatedly stimulating the test site itself. The sensitization of tail-withdrawal responses is associated with enhanced activation of the tail motor neurons and heterosynaptic facilitation of the monosynaptic connections between the tail sensory neurons and tail motor neurons. This synaptic facilitation can occur under conditions in which neither posttetanic potentiation nor generalized changes in postsynaptic input resistance contribute to the facilitation. In addition to producing monosynaptic excitatory postsynaptic potentials (EPSPs), action potentials in tail sensory neurons often recruit longer latency polysynaptic input to the tail motor neurons during sensitization. Strong, noxious tail shock similar in intensity to that used previously for sensitization and aversive classical conditioning of other responses in Aplysia produces more heterosynaptic facilitation than does weak sensitizing stimulation. Heterosynaptic facilitation builds up progressively with multiple trials and lasts for hours. Very strong shocks to the tail can change the response characteristics of tail sensory neurons so that a prolonged, regenerative burst of spikes is elicited by a brief intracellular depolarizing pulse. This bursting response produced by sensitizing stimulation has not been described previously in Aplysia sensory neurons and can greatly amplify the synaptic input to tail motor neurons from the sensory neurons. In addition, strong shocks to the tail increase the duration and magnitude of individual sensory neuron action potentials. Sensitizing tail stimulation usually produces long-lasting depolarization of the tail motor neurons and often long-lasting hyperpolarization of the tail sensory neurons. The tail motor and sensory neurons show both increases and decreases of input resistance following sensitizing stimulation. However, the small, occasional increases in input resistance of the motor neuron are insufficient to explain the heterosynaptic facilitation produced by sensitizing stimulation. Serotonin (5-HT) application can mimic many of the effects of sensitizing tail shock, including facilitation of both tail withdrawal and the monosynaptic connections between tail sensory and motor neurons, hyperpolarizing and depolarizing responses in the tail sensory neurons, and an increase in the duration and magnitude of the sensory neuron action potential. In the nearly isolated sensory neuron soma, 5-HT usually produces a slow, decreased conductance depolarizing response, suggesting that the 5-HT-induced hyperpolarizing response see Copyright © 1983 the American Physiological Society

Gebhart, G. F.; Sandkuhler, J.; Thalhammer, J. G.; Zimmermann, M.

doi: N/Apmid: 6663337

Abstract The organization in the brain stem of descending inhibitory control of spinal nociceptive information was studied in anesthetized, paralyzed cats by quantitatively evaluating the effects of reversible blocks produced by lidocaine microinjected in the medial and/or lateral medulla. Spinal neuronal inhibition produced by stimulation in the nucleus raphe magnus (NRMS) was compared to the inhibition of the same dorsal horn neurons produced by stimulation 2 mm lateral in the medullary reticular formation (MRFS). When the inhibition produced by NRMS and/or MRFS was blocked by lidocaine microinjected in those medullary sites, the efficacy of spinal neuronal inhibition produced by stimulation in the midbrain periaqueductal gray (PAGS) and 4 mm lateral in the reticular formation (LRFS) was evaluated and compared with the inhibition produced before the intramedullary microinjection of lidocaine. All 32 spinal dorsal horn neurons studied responded to hindlimb cutaneous nerve stimulation at strengths supramaximal for activation of A-alpha,delta- and C-fibers, to mechanical stimuli applied to the skin, and 27 also responded to noxious radiant heating (50 degrees C, 10 s) of the skin of the foot- or toepads (5 units had receptive fields in the hairy skin of the hindlimb). The noxious heat-evoked responses of all units studied were inhibited by NRMS or MRFS. The mean threshold currents for spinal inhibition, the mean maximal inhibition produced, and the mean stimulation currents producing an attenuation to 50% of the control response to 50 degrees C skin heating did not differ between NRMS and MRFS. When quantitatively compared on the same spinal units, NRMS produced the same mean magnitude of inhibition as the same intensities of MRFS, and both NRMS and MRFS produced the same mean percent increment in inhibition per 100-microA increase in the intensity of brain stimulation. The responses of the spinal units studied to graded noxious heating of the skin was a monotonic linear function throughout the temperature range employed (42-50 degrees C). MRFS shifted this stimulus response function (SRF) to the right, raising significantly the threshold of response a mean 2.2 degrees C to noxious heating of the skin without significantly affecting the slope of the SRF. MRFS reduced the number of discharges of spinal units evoked by electrical A-alpha,beta-fiber stimulation of hindlimb cutaneous nerves in 4 of 10 units studied. NRMS similarly inhibited the A-alpha,beta-fiber-evoked responses of two of the same four units affected by MRFS but also affected two of the remaining six units not affected by MRFS.(ABSTRACT TRUNCATED AT 400 WORDS) Copyright © 1983 the American Physiological Society

Richmond, B. J.; Wurtz, R. H.; Sato, T.

doi: N/Apmid: 6663335

Abstract We studied the responses to visual stimuli of neurons in area TE of the inferior temporal (IT) cortex in four awake monkeys (Macaca mulatta) trained to perform behavioral tasks. While the monkey looked at a fixation point in order to detect its dimming, another stimulus, such as a spot of light or a sine- or square-wave grating, usually produced only slight responses in inferior temporal neurons. However, the response to the stimulus was more vigorous if the task was changed so the fixation point blinked off before the stimulus came on while the monkey maintained its gaze. Responses to visual stimuli during this blink task were seen in 199 of 288 cells studied, and nearly all responded to a visual stimulus better during the blink task than during the task in which the fixation point remained on. Small spots of light usually produced consistent responses; we did not explore the response to complex stimuli or to objects. Latency of the visual response ranged from 70 to 220 ms. While the response of cells to a stimulus in the presence of the fixation point was limited to areas near the fovea, this apparently constricted visual receptive field expanded during the blink of the fixation point. In order to determine whether the increased response of the cell in the absence of the fixation point was due to a shift of attention from the fixation point to the visual stimulus, we required the monkey to respond to the dimming of this stimulus rather than to the dimming of the fixation point. We found that attention to the visual stimulus decreased the response of the cell during both the fixation and blink tasks. That is, the best response to the stimulus occurred in the blink task when attention to the stimulus was not required, while the poorest response occurred in the fixation task when attention to the stimulus was required. The reappearance of the fixation point during stimulus presentation in the blink task caused a transient time-locked suppression of response to the stimulus. This suggests that the reduction of response to the stimulus in the presence of the fixation point is caused by an interaction between the responses to the fixation point and the visual stimulus. To insure that we were recording from the same population of cells that had first been characterized by Gross, Rocha-Miranda, and Bender (14) in anesthetized, paralyzed monkeys, we recorded under those same conditions in two of our four monkeys.(ABSTRACT TRUNCATED AT 400 WORDS) Copyright © 1983 the American Physiological Society

Langmoen, I. A.; Andersen, P.

doi: N/Apmid: 6663329

Abstract The summation of excitatory postsynaptic potentials (EPSPs) generated in separate parts of the dendritic tree of hippocampal pyramidal cells has been investigated using the in vitro slice preparation. Two separate inputs with known synaptic location were used. The EPSP produced by simultaneous activation of the two inputs (observed sum) was compared to the algebraic sum of the individual EPSPs. Small-amplitude EPSPs (0.5-1.5 mV) added linearly. The shortest distance between the two synaptic groups was 75 micron. With larger amplitudes (greater than 2.5 mV), the EPSP summated nonlinearly. The nonlinear summation was reduced by moderate hyperpolarizations (2-10 mV) of the soma membrane. Also, large EPSPs (greater than 2.5 mV) summated linearly when the peak of the summed EPSP was brought close to the equilibrium potential for the inhibitory postsynaptic potential (IPSP) (EIPSP). When the EPSP peak was made more negative than the EIPSP, summation was again nonlinear but the algebraic sum was now smaller than the observed EPSP sum, i.e., the direction of the nonlinearity was reversed. EPSP summation was linear after the IPSP had been blocked by benzyl penicillin application. We conclude that separate EPSPs in hippocampal pyramids (minimal separation, 75 micron) add linearly but that the addition of an IPSP may complicate this picture. No evidence was found for interaction between the different populations of excitatory synapses. Copyright © 1983 the American Physiological Society

Gebhart, G. F.; Sandkuhler, J.; Thalhammer, J. G.; Zimmermann, M.

doi: N/Apmid: 6663336

Abstract The descending inhibition of spinal neuronal responses by focal electrical stimulation in the periaqueductal gray (PAG) or nucleus raphe magnus (NRM) was quantitatively studied and compared in the anesthetized, paralyzed cat. All 60 dorsal horn neurons studied were driven by electrical stimulation of hindlimb cutaneous nerves at strengths supramaximal for activation of A-alpha,delta- and C-fibers, and 52 also responded to noxious radiant heating (50 degrees C, 10 s) of the skin of the foot- or toepads; 8 units had receptive fields in the hairy skin of the hindlimb. All neurons studied also responded to mechanical stimuli; recording sites were located in laminae I-VI of the dorsal horn. The inhibition of spinal neuronal heat-evoked responses by stimulation in the PAG or NRM differed quantitatively when examined on the same spinal neurons. Inhibition of heat-evoked spinal neuronal responses occurred at a lower threshold of stimulation in the NRM than in the PAG. The mean intensity of stimulation in the NRM producing an attenuation to 50% of the control 50 degrees C heat-evoked response was significantly lower than the mean intensity of stimulation in the PAG producing a 50% attenuation of the same spinal units. The mean magnitude of inhibition produced by stimulation in the NRM was significantly greater than that produced on the same spinal units by the same intensity of stimulation in the PAG. However, stimulation in the NRM and PAG produced the same mean percent change in inhibition per 100-microA increase in the intensity of stimulation. Thus, the slopes of the recruitment of descending inhibition from the PAG and the NRM as a function of increasing intensities of stimulation are the same; the lines of recruitment of inhibition are parallel. When examined on the same dorsal horn units, stimulation in the PAG influenced their intensity coding to graded noxious heating of the skin differently than did stimulation in the NRM. The responses of the class 2 and class 3 spinal units examined to increasing temperatures of heat applied to the skin was a monotonic linear function throughout the temperature range studied (42-50 degrees C). Stimulation in the PAG decreased the slope of the stimulus-response function (SRF) without affecting unit thresholds of response, thus influencing the gain control of nociceptive transmission in the dorsal horn. Stimulation in the NRM produced a parallel shift to the right of the SRF, influencing the set point and threshold of response.(ABSTRACT TRUNCATED AT 400 WORDS) Copyright © 1983 the American Physiological Society

Wolpaw, J. R.; Braitman, D. J.; Seegal, R. F.

doi: N/Apmid: 6663327

Abstract Description of the neuronal and synaptic bases of memory in the vertebrate central nervous system (CNS) requires a CNS stimulus-response pathway that is defined and accessible, has the capacity for adaptive change, and clearly contains the responsible substrates. This study was an attempt to determine whether the spinal stretch reflex (SSR), the initial, purely spinal, portion of the muscle stretch response, which satisfies the first requirement, also satisfies the second, capacity for adaptive change. Monkeys prepared with chronic fine-wire biceps electromyographic (EMG) electrodes were trained to maintain elbow position and a given level of biceps background EMG activity against constant extension torque. At random times, a brief additional extension torque pulse extended the elbow and elicited the biceps SSR. Under the control mode, reward always followed. Under the SSR increases or SSR decreases mode, reward followed only if the absolute value of biceps EMG from 14 to 24 ms after stretch onset (the SSR interval) was above or below a set value. Animals performed 3,000-6,000 trials/day over data-collection periods of up to 15 mo. Background EMG and the initial 30 ms of pulse-induced extension remained stable throughout data collection. Under the SSR increases or SSR decreases mode, SSR amplitude (EMG amplitude in the SSR interval minus background EMG amplitude) changed appropriately. Change was evident in 5-10 days and progressed over at least 4 wk. The SSR increased (SSR increases) to 140-190% control amplitude or decreased (SSR decreases) to 22-79%. SSR change did not regress over 12-day gaps in task performance. A second pair of biceps electrodes, monitored simultaneously, supplied comparable data, indicating that SSR amplitude change occurred throughout the muscle. Beyond 40 ms after pulse onset, elbow extension was inversely correlated with SSR amplitude. The delay between the SSR and its apparent effect on movement is consistent with expected motor-unit contraction time. The data demonstrate that the SSR is capable of adaptive change. At present the most likely site(s) of the mechanism of SSR amplitude change are the Ia synapse and/or the muscle spindle. Available related evidence suggests persistent segmental change may in fact come to mediate SSR amplitude change. If so, such segmental change would constitute a technically accessible fragment of a memory. Copyright © 1983 the American Physiological Society

Walters, E. T.; Byrne, J. H.; Carew, T. J.; Kandel, E. R.

doi: N/Apmid: 6663341

Abstract Mechanical, chemical, or electrical stimulation of the tail elicits a short-latency (less than 1 s) tail-withdrawal reflex that is graded with the intensity of the stimulus. The tail-withdrawal reflex is not elicited by stimulation of parts of the body outside of the tail region. Mechanoafferent neurons innervating the tail are located in a small subcluster within a large, homogeneous group of medium-size (40-80 micron) cells on the ventrocaudal (VC) surface of each pleural ganglion. The tail sensory neurons within this large VC cluster are activated by tactile pressure or by electrical stimulation of discrete regions of the tail. They adapt slowly to maintained stimulation and sometimes respond to stimulus offset as well. Both mechanical and electrical stimuli produce responses that are graded with the intensity of the stimulus. Cells in the VC cluster appear to be primary mechanoreceptors because they have axons in peripheral nerves (including nerves innervating the tail), they exhibit action potentials lacking prepotentials in response to tactile stimulation, and these action potentials are still produced by cutaneous stimulation when peripheral and central chemical synaptic transmission is blocked. Stimulation of fields all over the body surface evokes synaptically mediated hyperpolarizing responses in individual mechanoafferent neurons that may represent afferent inhibition. Hyperpolarizing responses lasting many seconds can be produced by brief cutaneous stimuli. The mechanoafferent neurons innervating the tail region make strong monosynaptic connections to tail motor neurons in the ipsilateral pedal ganglion, and through these connections this subpopulation of the VC neurons appears to make a substantial contribution to the short-latency tail-withdrawal reflex. In addition, the combined excitatory receptive fields of these mechanoafferents match the excitatory receptive field of the tail-withdrawal reflex. Mechanoafferent neurons in the VC cluster that have receptive fields on other parts of the body (outside the excitatory receptive field of the tail-withdrawal reflex) have not been observed to make monosynaptic connections to the tail motor neurons. The neurons innervating the tail are reliably found in a discrete region within the larger VC cluster. In addition to this gross somatotopic organization, there is evidence of a finer level of somatotopic organization between the position of the excitatory receptive field on the tail and the position of the cell soma in the tail subcluster.(ABSTRACT TRUNCATED AT 400 WORDS) Copyright © 1983 the American Physiological Society

Frishman, L. J.; Schweitzer-Tong, D. E.; Goldstein, E. B.

doi: N/Apmid: 6663334

Abstract Velocity tuning curves were measured for on-center cells in the dorsal lateral geniculate nucleus of the cat using a stimulus approximately the height and one-fourth the width of the hand-plotted receptive-field center. The standard stimulus strength was 1 log unit above the mesopic background luminance. Lateral geniculate Y-cells had significantly higher preferred velocities than geniculate X-cells when cells with receptive fields having the same range of retinal eccentricities were compared. Preferred velocity increased for both classes of cells as a function of retinal eccentricity. For all geniculate cells, preferred velocity increased with stimulus strength, showing an approximately threefold increase in preferred velocity for each log unit of stimulus strength. Preferred velocity was measured for on-center retinal ganglion cells with receptive fields at the same range of retinal eccentricities as the geniculate sample and under the same stimulus conditions. Preferred velocities of retinal ganglion Y-cells were significantly higher than those of ganglion X-cells, and as for geniculate cells, preferred velocities increased with increasing stimulus strength. However, the classes were better separated in the geniculate than in the retina; with geniculate X-cells having lower preferred velocities than retinal X-cells, and the geniculate Y-cells having higher preferred velocities than retinal Y-cells. For retinal ganglion cells, smaller receptive-field center sizes of the X-cells than the Y-cells could account in large part for the lower preferred velocities of the X-cells. However, for geniculate cells, differences in receptive-field center size could not account as well for the differences in preferred velocity between X- and Y-cells. Furthermore, field size differences could not account for the differences in preferred velocity between ganglion and geniculate cells of the same functional class. Experiments comparing responses to moving stimuli and flashed stationary stimuli show that stimuli moving at high velocities are in effect equivalent to brief-duration flashes, and responses are governed by the same laws of temporal summation in both cases. When velocity tuning curves were measured with long bars that enhanced peripheral inhibition, geniculate X- and Y-cells were better separated than ganglion X- and Y-cells, not only with respect to preferred velocity but also, with respect to velocity selectivity (width of the velocity tuning curve) and differential velocity sensitivity (slope of the leg of the velocity tuning curves ascending from low velocities to the peak).(ABSTRACT TRUNCATED AT 400 WORDS) Copyright © 1983 the American Physiological Society