Journal of Neurophysiology

Nakagawa, Hideki; Matsumoto, Nobuyoshi

doi: N/Apmid: 9772247

Abstract Nakagawa, Hideki and Nobuyoshi Matsumoto. on and off channels of the frog optic tectum revealed by current source density analysis. J. Neurophysiol. 80: 1886–1899, 1998. The spatiotemporal patterns of excitatory synaptic activity in response to diffuse light on and off stimuli were examined by means of current source density (CSD) analysis. The qualitative and quantitative analyses obtained from 24 depth profiles for each stimulus revealed obviously different distributions of synaptic activity in the laminar structure. Two or three dominant current sinks I, II, and III were evoked in response to diffuse light on stimulation. Sink I was observed at the bottom of the retinorecipient layer. Both sinks II and III, showing an identical spatial pattern, were observed just above sink I. On the other hand, diffuse light off stimulation elicited up to six current sinks IV, V, VI, VII, VIII, and IX. Sink IV was observed at the bottom of the retinorecipient layer. Sink V was observed in the most superficial layer. Both sinks VI and VIII were located between the two preceding sinks. Finally, sinks VII and IX occurred below the retinorecipient layer. Five electrically evoked current sinks A, B, C, D, and E, characterized in our previous study, were also recognized in the present quantitative analysis. A statistical analysis revealed that, in visually evoked responses, statistical differences in the spatial distribution were not present between sinks I and IV, and sinks II and VIII ( P < 0.05). The analysis also showed that, in electrically evoked responses, only a pair of sinks C and E exhibit virtually identical spatial distribution ( P < 0.05). Based on well-known properties of the retinal ganglion cells, possible neuronal mechanisms underlying each of current sinks in the on and off channels and their functional meanings were considered. Sink I reflects the excitatory monosynaptic activity derived from R3 retinal ganglion cells. Sink IV reflects the excitatory monosynaptic activity derived from both R3 and R4 cells. Sinks V, VI, VII, and IX may be composed of successive polysynaptic excitatory potentials derived from convergence of inputs from both R3 and R4 cells. We concluded that the early four sinks play in particular an important role in eliciting avoidance behavior. On the other hand, sinks II, III, and VIII reflect excitatory synaptic activities derived from on - off retinal fibers of another type having slow conduction velocity. These late current sinks were suggested to mediate prey catching and its facilitation. Footnotes Address reprint requests to H. Nakagawa. Copyright © 1998 the American Physiological Society

Tate, Andrew K.; Malpeli, Joseph G.

doi: N/Apmid: 9772272

Abstract Tate, Andrew K. and Joseph G. Malpeli. Effects of focal inactivation of dorsal or ventral layers of the lateral geniculate nucleus on cats' ability to see and fixate small targets. J. Neurophysiol. 80: 2206–2209, 1998. To reveal contributions of different subdivisions of the lateral geniculate nucleus (LGN) to visuomotor behavior, segments of either layer A or the C layers were inactivated with microinjections of γ-aminobutyric acid while cats made saccades to retinally stabilized spots of light placed either in affected regions of visual space or mirror-symmetric locations in the opposite hemifield. Inactivating layer A reduced the success rate for saccades to targets presented in affected locations from 82.4 to 26.8% while having no effect on saccades to the control hemifield. Saccades to affected sites had reduced accuracy and longer initiation latency and tended to be hypometric. In contrast, inactivating C layers did not affect performance. Data from all conditions fell along the same saccade velocity/amplitude function (“main sequence”), suggesting that LGN inactivations cause localization deficits, but do not interfere with saccade dynamics. Cerebral cortex is the only target of the A layers, so behavioral decrements caused by inactivating layer A must be related to changes in cortical activity. Inactivating layer A substantially reduces the activity of large subsets of corticotectal cells in areas 17 and 18, whereas few corticotectal cells depend on C layers for visually driven activity. The parallels between these behavioral and electrophysiological data along with the central role of the superior colliculus in saccadic eye movements suggests that the corticotectal pathway is involved in both deficits and remaining capacities resulting from blockade of layer A.

Thier, Peter; Andersen, Richard A.

doi: N/Apmid: 9772234

Abstract Thier, Peter and Richard A. Andersen. Electrical microstimulation distinguishes distinct saccade-related areas in the posterior parietal cortex. J. Neurophysiol. 80: 1713–1735, 1998. Electrical microstimulation (0.1-ms bipolar pulses at 500 Hz, current strength usually between 100 and 200 μA) was used to delineate saccade-related areas in the posterior parietal cortex of monkeys. Stimulation-induced saccades were found to be restricted to the lateral intraparietal area (area LIP) in the intraparietal sulcus (IPS) and a region on the medial aspect of the parietal lobe (area MP, medial parietal area), close to the caudal end of the cingulate sulcus, whereas stimulation of area 7a did not evoke eye movements. Two different types of evoked saccades were observed. Modified vector saccades, whose amplitude was modified by the position of the eyes at stimulation onset were the hallmark of sites in area LIP and area MP. The same sites were characterized by a propensity of single units active in the memory and presaccadic response segments of the memory saccade paradigm. Goal-directed saccades driving the eyes toward a circumscribed region relative to the head were largely restricted to a small strip of cortex on the lateral bank and the floor of the IPS (the intercalated zone), separating the representation of upward and downward directed saccades in LIP. Unlike stimulation in LIP or MP, stimulation in the intercalated zone gave rise to head, pinnae, facial, and shoulder movements accompanying the evoked saccades. We propose that the amplitude modification of vector saccades characterizing LIP and MP may reflect a spatially distributed head-centered coding scheme for saccades. On the other hand, the goal-directed saccades found in the intercalated zone could indicate the use of a spatially much more localized representation of desired location in head-centered space. Footnotes Address for reprint requests: P. Thier, Neurologische Universitätsklinik, Sektion für Visuelle Sensomotorik, Hoppe-Seyler-Str. 3, 72076 Tübingen, Germany. Present address of R. A. Andersen: California Institute of Technology, Pasadena, CA 91125. Copyright © 1998 the American Physiological Society

Chen, Gong; van den Pol, Anthony N.

doi: N/Apmid: 9772250

Abstract Chen, Gong and Anthony N. van den Pol. Coexpression of multiple metabotropic glutamate receptors in axon terminals of single suprachiasmatic nucleus neurons. J. Neurophysiol. 80: 1932–1938, 1998. Glutamate is the primary excitatory transmitter in axons innervating the hypothalamic suprachiasmatic nucleus (SCN) and is responsible for light-induced phase shifts of circadian rhythms generated by the SCN. By using self-innervating single neuron cultures and patch-clamp electrophysiology, we studied metabotropic glutamate receptors (mGluRs) expressed by SCN neurons. The selective agonists for group I (3,5-dihydroxy-phenylglycine), group II ((S)-4-carboxy-3-hydroxyphenylglycine), and group III ( l (+)-2-amino-4-phosphonobutyric acid) mGluRs all depressed the evoked IPSC in a subset (33%) of single autaptic neurons, suggesting a coexpression of all three groups of mGluRs in the same axon terminals of a single neuron. Other neurons showed a variety of combinations of mGluRs, including an expression of only one group of mGluR (18%) or coexpression of two groups of mGluRs (27%). Some neurons had no response to any of the three agonists (22%). The three mGluR agonists had no effect on postsynaptic γ-aminobutyric acid (GABA) receptor responses, indicating a presynaptic modulation of GABA release by mGluRs. We conclude that multiple mGluRs that act through different second messenger pathways are coexpressed in single axon terminals of SCN neurons where they modulate the release of GABA presynaptically, usually inhibiting release. Footnotes Address for reprint requests; A. van den Pol, Department of Neurosurgery, Yale University School of Medicine, 333 Cedar St., New Haven, CT 06520. Present address of G. Chen: Department of Molecular and Cellular Physiology, Beckman Center, B101, Stanford University Medical School, Stanford, CA 94305.

Green, Andrea M.; Galiana, Henrietta L.

doi: N/Apmid: 9772275

Abstract Green, Andrea M. and Henrietta L. Galiana. Hypothesis for shared central processing of canal and otolith signals. J. Neurophysiol. 80: 2222–2228, 1998. A common goal of the translational vestibuloocular reflex (TVOR) and the rotational vestibuloocular reflex (RVOR) is to stabilize visual targets on the retinae during head movement. However, these reflexes differ significantly in their dynamic characteristics at both sensory and motor levels, implying a requirement for different central processing of canal and otolith signals. Semicircular canal afferents carry a signal proportional to angular head velocity, whereas primary otolith afferents modulate approximately in phase with linear head acceleration. Behaviorally, the RVOR exhibits a robust response down to ∼0.01 Hz, yet the TVOR is only significant above ∼0.5 Hz. Several hypotheses were proposed to address central processing in the TVOR pathways. All rely on a central filtering process that precedes a “neural integrator” shared with the RVOR. We propose an alternative hypothesis for the convergence of canal and otolith signals that does not impose the requirement for additional low-pass filters for the TVOR. The approach is demonstrated using an anatomically based, simple model structure that reproduces the general dynamic characteristics of the RVOR and TVOR at both ocular and central levels. Differential dynamic processing of otolith and canal signals is achieved by virtue of the location at which sensory information enters a shared but distributed neural integrator. As a result, only the RVOR is provided with compensation for the eye plant. Hence canal and otolith signals share a common central integrator, as in previous hypotheses. However, we propose that the required additional filtering of otolith signals is provided by the eye plant. Footnotes Address for reprint requests: H. L. Galiana, Dept. of Biomedical Engineering, McGill University, 3775 University St., Montreal, Quebec H3A 2B4, Canada. Copyright © 1998 the American Physiological Society

White, Andrew J. R.; Wilder, Heath D.; Goodchild, Ann K.; Sefton, Ann Jervie; Martin, Paul R.

doi: N/Apmid: 9772261

Abstract White, Andrew J. R., Heath D. Wilder, Ann K. Goodchild, Ann Jervie Sefton, and Paul R. Martin. Segregation of receptive field properties in the lateral geniculate nucleus of a New-World monkey, the marmoset Callithrix jacchus . J. Neurophysiol. 80: 2063–2076, 1998. The lateral geniculate nucleus (LGN) in humans and Old-World monkeys is dominated by the representation of the fovea in the parvocellular (PC) layers, and most PC cells in the foveal representation have red–green cone opponent receptive field properties. It is not known whether these features are both unique to trichromatic primates. Here we measured receptive field properties and the visuotopic organization of cells in the LGN of a New-World monkey, the marmoset Callithrix jacchus . The marmoset displays a polymorphism of cone opsins in the medium-long wavelength (ML) range, which allows the LGN of dichromatic (“red–green color blind”) and trichromatic individuals to be compared. Furthermore, the koniocellular–interlaminar layers are segregated from the main PC layers in marmoset, allowing the functional role of this subdivision of the LGN to be assessed. We show that the representation of the visual field in the LGN is quantitatively similar in dichromatic and trichromatic marmosets and is similar to that reported for macaque; the vast majority of LGN volume is devoted to the central visual field. on - and off -type responses are partially segregated in the PC layers so that on responses are more commonly encountered near the external border of each layer. The red–green (ML) opponent cells in trichromatic animals were all located in the PC layers, and their receptive fields were within 16° of the fovea. The koniocellular zone between the PC and magnocellular layers contained cells that receive excitatory input from short wavelength sensitive cones (“blue- on cells”) as well as other nonopponent cells. These results suggest that the basic organization of the LGN is common to dichromatic and trichromatic primates and provide further evidence that ML and SWS opponent signals are carried in distinct subdivisions of the retinogeniculocortical pathway. Footnotes Address for reprint requests: P. R. Martin, Dept. Physiology F13, University of Sydney, NSW 2006, Australia.

Roska, Botond; Gaal, Lubor; Werblin, Frank S.

doi: N/Apmid: 9772252

Abstract Roska, Botond, Lubor Gaal, and Frank S. Werblin. Voltage-dependent uptake is a major determinant of glutamate concentration at the cone synapse: an analytical study. J. Neurophysiol. 80: 1951–1960, 1998. It was suggested that glutamate concentration at the synaptic terminal of the cones was controlled primarily by a voltage-dependent glutamate transporter and that diffusion played a less important role. The conclusion was based on the observation that the rate of glutamate concentration during the hyperpolarizing light response was dramatically slowed when the transporter was blocked with dihydrokainate although diffusion remained intact. To test the validity of this notion we constructed a model in which the balance among uptake, diffusion, and release determined the flow of glutamate into and out of the synaptic cleft. The control of glutamate concentration was assumed here to be determined by two relationships; 1 ) glutamate concentration is the integral over the synaptic volume of the rates of release, uptake, and diffusion, and 2 ) membrane potential is the integral over the membrane capacitance of the dark, leak, and transporter-gated chloride current. These relationships are interdependent because glutamate uptake via the transporter is voltage dependent and because the transporter-gated current is concentration dependent. The voltage and concentration dependence of release and uptake, as well as the light-elicited, transporter-gated, and leak currents were measured in other studies. All of these measurements were incorporated into our predictive model of glutamate uptake. Our results show a good quantitative fit between the predicted and the measured magnitudes and rates of change of glutamate concentration, derived from the two interdependent relationships. This close fit supports the validity of these two relationships as descriptors of the mechanisms underlying the control of glutamate concentration, it verifies the accuracy of the experimental data from which the functions used in these relationships were derived, and it lends further support to the notion that glutamate concentration is controlled primarily by uptake at the transporter. Footnotes Address for reprint requests: F. Werblin, 145 Life Sciences Addition, University of California, Berkeley, CA 94720.

Sohal, Vikaas S.; Huguenard, John R.

doi: N/Apmid: 9772235

Abstract Sohal, Vikaas S. and John R. Huguenard. Long-range connections synchronize rather than spread intrathalamic oscillations: computational modeling and in vitro electrophysiology. J. Neurophysiol. 80: 1736–1751, 1998. A thalamic network model was developed based on recent data regarding heterogeneous thalamic reticular (RE) cell axonal arborizations that indicate at least two projection patterns, short-range cluster projections and long-range diffuse projections. The model was constrained based on expected convergence and the biophysical properties of RE and thalamocortical (TC) cells and their synapses. The model reproduced in vitro synchronous slow (3-Hz) oscillatory activity and the known effects of T-channel blockade and cholecystokinin (CCK) application on this activity. Whereas previous models used the speed at which ≈3-Hz oscillations propagate in vitro to infer the spatial extent of intrathalamic projections, we found that, so long as the γ-aminobutyric acid-B synaptic conductance was adjusted appropriately, a network with only short-range projections and another network with both short- and long-range projections could both produce physiologically realistic propagation speeds. Although the ≈3-Hz oscillations propagated at similar speeds in both networks, phase differences between oscillatory activity at different locations in the network were much smaller in the network containing both short- and long-range projections. We measured phase differences in vitro and found that they were similar to those that arise in the network containing both short- and long-range projections but are inconsistent with the much larger phase differences that occur in the network containing only short-range projections. These results suggest that, although they extend much further than do short-range cluster projections, long-range diffuse projections do not spread activity over greater distances or increase the speed at which intrathalamic oscillations propagate. Instead, diffuse projections may function to synchronize activity and minimize phase shifts across thalamic networks. One prediction of this hypothesis is that, immediately after a collision between propagating oscillations, phase gradients should vary smoothly across the thalamic slice. The model also predicts that phase shifts between oscillatory activity at different points along a thalamic slice should be unaffected by T-channel blockers and decreased by suppression of synaptic transmission or application of CCK. Footnotes Address reprint requests to J. R. Huguenard.

Doeringer, Joseph A.; Hogan, Neville

doi: N/Apmid: 9772239

Abstract Doeringer, Joseph A. and Neville Hogan. Intermittency in preplanned elbow movements persists in the absence of visual feedback. J. Neurophysiol. 80: 1787–1799, 1998. It has been observed for nearly 100 years that visually guided human movements appear to be composed of submovements, intermittently executed overlapping segments. This paper presents experiments to investigate the pervasiveness of movement intermittency and, in particular, whether it is exclusively due to visual feedback. With and without visual feedback, human subjects were asked to 1 ) move with constant velocity and 2 ) draw elliptical figures on a phase-plane display (showing velocity vs. position) that required cyclic movements at different frequencies. In both tasks, we found that removal of visual feedback did not significantly change movement intermittency. Subjects were unable to generate movements at constant speed. In addition, subjects moved less smoothly when drawing slower phase-plane ellipses. Furthermore, elliptical phase-plane figures were not always drawn at the frequency suggested by the center of the display. Instead, subjects moved more slowly than the tall (fast) ellipse displays suggested, and faster than the wide (slow) displays suggested. These results show that 1 ) movement intermittency is not exclusively due to visual feedback and 2 ) may in fact be a fundamental feature of movement behavior. Footnotes Address for reprint requests: J. A. Doeringer, Dept. of Mechanical Engineering, MIT, Rm. 3-147, 77 Massachusetts Ave., Cambridge, MA 02139.

Grasso, R.; Bianchi, L.; Lacquaniti, F.

doi: N/Apmid: 9772246

Abstract Grasso, R., L. Bianchi, and F. Lacquaniti. Motor patterns for human gait: backward versus forward locomotion. J. Neurophysiol. 80: 1868–1885, 1998. Seven healthy subjects walked forward (FW) and backward (BW) at different freely chosen speeds, while their motion, ground reaction forces, and electromyographic (EMG) activity from lower limb muscles were recorded. We considered the time course of the elevation angles of the thigh, shank, and foot segments in the sagittal plane, the anatomic angles of the hip, knee, and ankle joints, the vertical and longitudinal ground reaction forces, and the rectified EMGs. The elevation angles were the most reproducible variables across trials in each walking direction. After normalizing the time course of each variable over the gait cycle duration, the waveforms of all elevation angles in BW gait were essentially time reversed relative to the corresponding waveforms in FW gait. Moreover, the changes of the thigh, shank, and foot elevation covaried along a plane during the whole gait cycle in both FW and BW directions. Cross-correlation analysis revealed that the phase coupling among these elevation angles is maintained with a simple reversal of the delay on the reversal of walking direction. The extent of FW–BW correspondence also was good for the hip angle, but it was smaller for the knee and ankle angles and for the ground reaction forces. The EMG patterns were drastically different in the two movement directions as was the organization of the muscular synergies measured by cross-correlation analysis. Moreover, at any given speed, the mean EMG activity over the gait cycle was generally higher in BW than in FW gait, suggesting a greater level of energy expenditure in the former task. We argue that conservation of kinematic templates across gait reversal at the expense of a complete reorganization of muscle synergies does not arise from biomechanical constraints but may reflect a behavioral goal achieved by the central networks involved in the control of locomotion. Footnotes Address for reprint requests: R. Grasso, Fisiologia umana, Istituto Scientifico Santa Lucia, Centre National de la Recherche, via Ardeatina 306, 00179 Roma, Italy. Copyright © 1998 the American Physiological Society