Journal of Neurophysiology

Isa, Tadashi; Hall, William C.

doi: 10.1152/jn.00498.2009pmid: 19710376

Abstract The superior colliculus plays an important role in the translation of sensory signals that encode the location of objects in space into motor signals that encode vectors of the shifts in gaze direction called saccades. Since the late 1990s, our two laboratories have been applying whole cell patch-clamp techniques to in vitro slice preparations of rodent superior colliculus to analyze the structure and function of its circuitry at the cellular level. This review describes the results of these experiments and discusses their contributions to our understanding of the mechanisms responsible for sensorimotor integration in the superior colliculus. The experiments analyze vertical interactions between its superficial visuosensory and intermediate premotor layers and propose how they might contribute to express saccades and to saccadic suppression. They also compare and contrast the circuitry within each of these layers and propose how this circuitry might contribute to the selection of the targets for saccades and to the build-up of the premotor commands that precede saccades. Experiments also explore in vitro the roles of extrinsic inputs to the superior colliculus, including cholinergic inputs from the parabigeminal and parabrachial nuclei and GABAergic inputs from the substantia nigra pars reticulata, in modulating the activity of the collicular circuitry. The results extend and clarify our understanding of the multiple roles the superior colliculus plays in sensorimotor integration. Footnotes Copyright © 2009 the American Physiological Society

Neri, Peter; Levi, Dennis

doi: 10.1152/jn.00489.2009pmid: 19726727

Abstract The response of motion-sensitive neurons to stimuli presented within their receptive field is often affected by stimulation in the surrounding region. These effects have perceptually relevant consequences that can be measured using behavioral techniques. We used psychophysical reverse correlation to characterize directional selectivity in human observers while they processed a local motion stimulus and studied the effect of adding an additional motion signal in the surrounding region. The surround had no effect on response gain for signals of opposite direction but selectively reduced gain for those of same direction. Surprisingly this reduction was close to 100%, effectively amounting to a gating process whereby signals of same direction were completely silenced. Our data indicate that by far the most prominent perceptual manifestation of center-surround antagonism is gain suppression by motion in the same direction without any appreciable change in directional tuning. Copyright © 2009 the American Physiological Society

Lim, Heejin; Wang, Yi; Xiao, Youping; Hu, Ming; Felleman, Daniel J.

doi: 10.1152/jn.91255.2008pmid: 19571184

Abstract V2 has long been recognized to contain functionally distinguishable compartments that are correlated with the stripelike pattern of cytochrome oxidase activity. Early electrophysiological studies suggested that color, direction/disparity, and orientation selectivity were largely segregated in the thin, thick, and interstripes, respectively. Subsequent studies revealed a greater degree of homogeneity in the distribution of response properties across stripes, yet color-selective cells were still found to be most prevalent in the thin stripes. Optical recording studies have demonstrated that thin stripes contain both color-preferring and luminance-preferring modules. These thin stripe color-preferring modules contain spatially organized hue maps, whereas the luminance-preferring modules contain spatially organized luminance-change maps. In this study, the neuronal basis of these hue maps was determined by characterizing the selectivity of neurons for isoluminant hues in multiple penetrations within previously characterized V2 thin stripe hue maps. The results indicate that neurons within the superficial layers of V2 thin stripe hue maps are organized into columns whose aggregated hue selectivity is closely related to the hue selectivity of the optically defined hue maps. These data suggest that thin stripes contain hue maps not simply because of their moderate percentage of hue-selective neurons, but because of the columnar and tangential organization of hue selectivity. Footnotes Copyright © 2009 the American Physiological Society

Yakushin, Sergei B.; Xiang, Yongqing; Cohen, Bernard; Raphan, Theodore

doi: 10.1152/jn.00245.2009pmid: 19692515

Abstract Little is known about the dependence of the roll angular vestibuloocular reflex (aVOR) on gravity or its gravity-dependent adaptive properties. To study gravity-dependent characteristics of the roll aVOR, monkeys were oscillated about a naso-occipital axis in darkness while upright or tilted. Roll aVOR gains were largest in the upright position and decreased by 7–15% as animals were tilted from the upright. Thus the unadapted roll aVOR gain has substantial gravitational dependence. Roll gains were also decreased or increased by 0.25 Hz, in- or out-of-phase rotation of the head and the visual surround while animals were prone, supine, upright, or in side-down positions. Gain changes, determined as a function of head tilt, were fit with a sinusoid; the amplitudes represented the amount of the gravity-dependent gain change, and the bias, the gravity-independent gain change. Gravity-dependent gain changes were absent or substantially smaller in roll (≈5%) than in yaw (25%) or pitch (17%), whereas gravity-independent gain changes were similar for roll, pitch, and yaw (≈20%). Thus the high-frequency roll aVOR gain has an inherent dependence on head orientation re gravity in the unadapted state, which is different from the yaw/pitch aVORs. This inherent gravitational dependence may explain why the adaptive circuits are not active when the head is tilted re gravity during roll aVOR adaptation. These behavioral differences support the idea that there is a fundamental difference in the central organization of canal-otolith convergence of the roll and yaw/pitch aVORs. Copyright © 2009 the American Physiological Society

Pliss, Lioudmila; Yang, Hua; Xu-Friedman, Matthew A.

doi: 10.1152/jn.00111.2009pmid: 19726731

Abstract Many synapses contain both AMPA receptors (AMPAR) and N -methyl- d -aspartate receptors (NMDAR), but their different roles in synaptic computation are not clear. We address this issue at the auditory nerve fiber synapse (called the endbulb of Held), which is formed on bushy cells of the cochlear nucleus. The endbulb refines and relays precise temporal information to nuclei responsible for sound localization. The endbulb has a number of specializations that aid precise timing, including AMPAR-mediated excitatory postsynaptic currents (EPSCs) with fast kinetics. Voltage-clamp experiments in mouse brain slices revealed that slow NMDAR EPSCs are maintained at mature endbulbs, contributing a peak conductance of around 10% of the AMPAR-mediated EPSC. During repetitive synaptic activity, AMPAR EPSCs depressed and NMDAR EPSCs summated, thereby increasing the relative importance of NMDARs. This could impact temporal precision of bushy cells because of the slow kinetics of NMDARs. We tested this by blocking NMDARs and quantifying bushy cell spike timing in current clamp when single endbulbs were activated. These experiments showed that NMDARs contribute to an increased probability of firing, shorter latency, and reduced jitter. Dynamic-clamp experiments confirmed this effect and showed it was dose-dependent. Bushy cells can receive inputs from multiple endbulbs. When we applied multiple synaptic inputs in dynamic clamp, NMDARs had less impact on spike timing. NMDAR conductances much higher than mature levels could disrupt spiking, which may explain its downregulation during development. Thus mature NMDAR expression can support the conveying of precise temporal information at the endbulb, depending on the stimulus conditions. Footnotes Copyright © 2009 the American Physiological Society

Asari, Hiroki; Zador, Anthony M.

doi: 10.1152/jn.00577.2009pmid: 19675288

Abstract Acoustic processing requires integration over time. We have used in vivo intracellular recording to measure neuronal integration times in anesthetized rats. Using natural sounds and other stimuli, we found that synaptic inputs to auditory cortical neurons showed a rather long context dependence, up to ≥4 s (τ ∼ 1 s), even though sound-evoked excitatory and inhibitory conductances per se rarely lasted ≳100 ms. Thalamic neurons showed only a much faster form of adaptation with a decay constant τ <100 ms, indicating that the long-lasting form originated from presynaptic mechanisms in the cortex, such as synaptic depression. Restricting knowledge of the stimulus history to only a few hundred milliseconds reduced the predictable response component to about half that of the optimal infinite-history model. Our results demonstrate the importance of long-range temporal effects in auditory cortex and suggest a potential neural substrate for auditory processing that requires integration over timescales of seconds or longer, such as stream segregation. Footnotes Copyright © 2009 the American Physiological Society

Mochizuki, Hideki; Inui, Koji; Tanabe, Hiroki C.; Akiyama, Lisa F.; Otsuru, Naofumi; Yamashiro, Koya; Sasaki, Akihiro; Nakata, Hiroki; Sadato, Norihiro; Kakigi, Ryusuke

doi: 10.1152/jn.00460.2009pmid: 19710378

Abstract Functional neuroimaging studies have identified itch-related brain regions. However, no study has investigated the temporal aspect of itch-related brain processing. Here this issue was investigated using electrically evoked itch in ten healthy adults. Itch stimuli were applied to the left wrist and brain activity was measured using magnetoencephalography (MEG) and functional magnetic resonance imaging (fMRI). In the MEG experiment, the magnetic responses evoked by the itch stimuli were observed in the contralateral and ipsilateral frontotemporal regions. The dipoles associated with the magnetic responses were mainly located in the contralateral (nine subjects) and ipsilateral (eight subjects) secondary somatosensory cortex (SII)/insula, which were also activated by the itch stimuli in the fMRI experiment. We also observed an itch-related magnetic response in the posterior part of the centroparietal region in six subjects. MEG and fMRI data showed that the magnetic response in this region was mainly associated with itch-related activation of the precuneus. The latency was significantly longer in the ipsilateral than that in the contralateral SII/insula, suggesting the difference to be associated with transmission in the callosal fibers. The timing of activation of the precuneus was between those of the contralateral and ipsilateral SII/insula. Other sources were located in the premotor, primary motor, and anterior cingulate cortices (one subject each). This study is the first to demonstrate part of the time course of itch-related brain processing. Combining methods with high temporal and spatial resolution (e.g., MEG and fMRI) would be useful to investigate the temporal aspect of the brain mechanism of itch. Copyright © 2009 the American Physiological Society

Frigon, Alain; Barrière, Grégory; Leblond, Hugues; Rossignol, Serge

doi: 10.1152/jn.00572.2009pmid: 19726726

Abstract Locomotion involves dynamic interactions between the spinal cord, supraspinal signals, and peripheral sensory inputs. After incomplete spinal cord injury (SCI), interactions are disrupted, and remnant structures must optimize function to maximize locomotion. We investigated if cutaneous reflexes are altered following a unilateral partial spinal lesion and whether changes are retained within spinal circuits after complete spinal transection (i.e., spinalization). Four cats were chronically implanted with recording and stimulating electrodes. Cutaneous reflexes were evoked with cuff electrodes placed around left and right superficial peroneal nerves. Control data, consisting of hindlimb kinematics and electromyography (bursts of muscular activity and cutaneous reflexes), were recorded during treadmill locomotion. After stable control data were achieved (53–67 days), a partial spinal lesion was made at the 10th or 11th thoracic segment (T 10 –T 11 ) on the left side. Cats were trained to walk after the partial lesion, and following a recovery period (64–80 days), a spinalization was made at T 13 . After the partial lesion, changes in short-latency excitatory (P1) homologous responses between hindlimbs, evoked during swing, were largely asymmetric in direction relative to control values, whereas changes in longer-latency excitatory (P2) and crossed responses were largely symmetric in direction. After spinalization, cats could display hindlimb locomotion within 1 day. Early after spinalization, reflex changes persisted a few days, but over time homologous P1 responses increased symmetrically toward or above control levels. Therefore changes in cutaneous reflexes after the partial lesion and retention following spinalization indicate an important spinal plasticity after incomplete SCI. Footnotes Copyright © 2009 the American Physiological Society