Journal of Neurophysiology

Dahiya, Ravinder S.; Gori, Monica

doi: 10.1152/jn.01007.2009pmid: 20393056

Abstract A recent report by Scheibert et al. highlights the role of fingerprints in enhancing tactile sensitivity. By scanning a surface with a biometric force sensor they demonstrate the dominance of the frequencies that fall within the optimal sensitivity range of Pacinian afferents. The sensor, in this study, has a soft cover patterned with parallel ridges—mimicking the fingerprints. However, the skin structure is quite complex. Elasticity of the skin varies with depth and the ridge like pattern is comprised of not just papillary ridges or fingerprints. Besides fingerprints there exist intermediate ridges, positioned exactly under the papillary ridges, and limiting ridges at dermis-epidermis junction. These structures are usually considered as single unit. If so, it is important to revisit and see if the role of fingerprints remains the same, should the sensor cover have both fingerprints and intermediate ridges. Copyright © 2010 The American Physiological Society

Rosen, Andrew M.; Sichtig, Heike; Schaffer, J. David; Di Lorenzo, Patricia M.

doi: 10.1152/jn.01098.2009pmid: 20445036

Abstract Although the cellular organization of many primary sensory nuclei has been well characterized, questions remain about the functional architecture of the first central relay for gustation, the rostral nucleus of the solitary tract (NTS). Here we used electrophysiological data recorded from single cells in the NTS to inform a network model of taste processing. Previous studies showed that electrical stimulation of the chorda tympani (CT) nerve initiates two types of inhibitory influences with different time courses in separate groups of NTS cells. Each type of inhibition targeted cells with distinct taste response properties. Further analyses of these data identified three NTS cell types differentiated by their latency of evoked response, time course of CT evoked inhibition, and degree of selectivity across taste qualities. Based on these results, we designed a model of the NTS consisting of discrete, reciprocally connected, stimulus-specific “cell” assemblies. Input to the network of integrate-and-fire model neurons was based on electrophysiological recordings from the CT nerve. Following successful simulation of paired-pulse CT stimulation, the network was tested for its ability to discriminate between two “taste” stimuli. Network dynamics of the model produced biologically plausible responses from each unit type and enhanced discrimination between taste qualities. We propose that an interactive network of taste quality specific cell assemblies, similar to our model, may account for the coherence in across-neuron patterns of NTS responses between similar tastants. Copyright © 2010 The American Physiological Society

Beurg, Maryline; Nam, Jong-Hoon; Chen, Qingguo; Fettiplace, Robert

doi: 10.1152/jn.00019.2010pmid: 20427623

Abstract Auditory transduction occurs by opening of Ca 2+ -permeable mechanotransducer (MT) channels in hair cell stereociliary bundles. Ca 2+ clearance from bundles was followed in rat outer hair cells (OHCs) using fast imaging of fluorescent indicators. Bundle deflection caused a rapid rise in Ca 2+ that decayed after the stimulus, with a time constant of about 50 ms. The time constant was increased by blocking Ca 2+ uptake into the subcuticular plate mitochondria or by inhibiting the hair bundle plasma membrane Ca 2+ ATPase (PMCA) pump. Such manipulations raised intracellular Ca 2+ and desensitized the MT channels. Measurement of the electrogenic PMCA pump current, which saturated at 18 pA with increasing Ca 2+ loads, indicated a maximum Ca 2+ extrusion rate of 3.7 fmol·s −1 . The amplitude of the Ca 2+ transient decreased in proportion to the Ca 2+ concentration bathing the bundle and in artificial endolymph (160 mM K + , 20 μM Ca 2+ ), Ca 2+ carried 0.2% of the MT current. Nevertheless, MT currents in endolymph displayed fast adaptation with a submillisecond time constant. In endolymph, roughly 40% of the MT current was activated at rest when using 1 mM intracellular BAPTA compared with 12% with 1 mM EGTA, which enabled estimation of the in vivo Ca 2+ load as 3 pA at rest. The results were reproduced by a model of hair bundle Ca 2+ diffusion, showing that the measured PMCA pump density could handle Ca 2+ loads incurred from resting and maximal MT currents in endolymph. The model also indicated the endogenous mobile buffer was equivalent to 1 mM BAPTA. Copyright © 2010 The American Physiological Society

Colgin, Laura L.; Leutgeb, Stefan; Jezek, Karel; Leutgeb, Jill K.; Moser, Edvard I.; McNaughton, Bruce L.; Moser, May-Britt

doi: 10.1152/jn.00202.2010pmid: 20445029

Abstract The autoassociative memory model of hippocampal field CA3 postulates that Hebbian associations among external input features produce attractor states embedded in a recurrent synaptic matrix. In contrast, the attractor-map model postulates that a two-dimensional continuum of attractor states is preconfigured in the network during development and that transitions among these states are governed primarily by self-motion information (“path-integration”), giving rise to the strong spatial characteristic of hippocampal activity. In this model, learned associations between “coordinates” on the attractor map and external cues can result in abrupt jumps between states, in the case of mismatches between the current input and previous associations between internal coordinates and external landmarks. Both models predict attractor dynamics, but for fundamentally different reasons; however, the two models are not a priori mutually exclusive. We contrasted these two models by comparing the dynamics of state transitions when two previously learned environmental shapes were morphed between their endpoints, in animals that had first experienced the environments either at the same location, or at two different locations, connected by a passageway through which they walked. As predicted from attractor-map theory, the latter animals expressed abrupt transitions between representations at the midpoint of the morph series. Contrary to the predictions of autoassociation theory, the former group expressed no evidence of attractor dynamics during the morph series; there was only a gradual transition between endpoints. The results of this critical test thus cast the autoassociator theory for CA3 into doubt and indicate the need for a new theory for this structure. Footnotes Copyright © 2010 The American Physiological Society

Fisher, Helen E.; Brown, Lucy L.; Aron, Arthur; Strong, Greg; Mashek, Debra

doi: 10.1152/jn.00784.2009pmid: 20445032

Abstract Romantic rejection causes a profound sense of loss and negative affect. It can induce clinical depression and in extreme cases lead to suicide and/or homicide. To begin to identify the neural systems associated with this natural loss state, we used functional magnetic resonance imaging to study 10 women and 5 men who had recently been rejected by a partner but reported they were still intensely “in love.” Participants alternately viewed a photograph of their rejecting beloved and a photograph of a familiar, individual, interspersed with a distraction-attention task. Their responses while looking at their rejecter included love, despair, good, and bad memories, and wondering why this happened. Activation specific to the image of the beloved occurred in areas associated with gains and losses, craving and emotion regulation and included the ventral tegmental area (VTA) bilaterally, ventral striatum, medial and lateral orbitofrontal/prefrontal cortex, and cingulate gyrus. Compared with data from happily-in-love individuals, the regional VTA activation suggests that mesolimbic reward/survival systems are involved in romantic passion regardless of whether one is happily or unhappily in love. Forebrain activations associated with motivational relevance, gain/loss, cocaine craving, addiction, and emotion regulation suggest that higher-order systems subject to experience and learning also may mediate the rejection reaction. The results show activation of reward systems, previously identified by monetary stimuli, in a natural, endogenous, negative emotion state. Activation of areas involved in cocaine addiction may help explain the obsessive behaviors associated with rejection in love. Copyright © 2010 The American Physiological Society

Kumano, Hironori; Uka, Takanori

doi: 10.1152/jn.00040.2010pmid: 20445031

Abstract Neurons in extrastriate visual areas have large receptive fields (RFs) compared with those in primary visual cortex (V1), suggesting extensive spatial integration. To examine the spatial integration of neurons in area MT, we modeled the RFs of MT neurons based on a symmetrical (Gaussian) integration of V1 outputs and tested the model using single-unit recording in two fixating macaque monkeys. Because visual representation in V1 is logarithmically compressed along eccentricity, the resulting RF model is log-Gaussian along the radial axis in polar coordinates. To test the log-Gaussian model, the RF of each neuron was mapped on a 5 × 5 grid using a small patch of random dots drifting at the preferred velocity of the neuron. The majority of MT neurons had RFs with a steeper slope near the fovea and a shallower slope away from the fovea. Among various two-dimensional Gaussian models fitted to the RFs, the log-Gaussian model provided the best description. The fitted parameters revealed that the range of sampling by MT neurons has no systematic relationship with eccentricities, consistent with a recent study for V4 neurons. Our results suggest that MT neurons integrate inputs from constant-sized patches of V1 cortex. Copyright © 2010 The American Physiological Society

Serences, John T.; Saproo, Sameer

doi: 10.1152/jn.01090.2009pmid: 20410360

Abstract Voluntary and stimulus-driven shifts of attention can modulate the representation of behaviorally relevant stimuli in early areas of visual cortex. In turn, attended items are processed faster and more accurately, facilitating the selection of appropriate behavioral responses. Information processing is also strongly influenced by past experience and recent studies indicate that the learned value of a stimulus can influence relatively late stages of decision making such as the process of selecting a motor response. However, the learned value of a stimulus can also influence the magnitude of cortical responses in early sensory areas such as V1 and S1. These early effects of stimulus value are presumed to improve the quality of sensory representations; however, the nature of these modulations is not clear. They could reflect nonspecific changes in response amplitude associated with changes in general arousal or they could reflect a bias in population responses so that high-value features are represented more robustly. To examine this issue, subjects performed a two-alternative forced choice paradigm with a variable-interval payoff schedule to dynamically manipulate the relative value of two stimuli defined by their orientation (one was rotated clockwise from vertical, the other counterclockwise). Activation levels in visual cortex were monitored using functional MRI and feature-selective voxel tuning functions while subjects performed the behavioral task. The results suggest that value not only modulates the relative amplitude of responses in early areas of human visual cortex, but also sharpens the response profile across the populations of feature-selective neurons that encode the critical stimulus feature (orientation). Moreover, changes in space- or feature-based attention cannot easily explain the results because representations of both the selected and the unselected stimuli underwent a similar feature-selective modulation. This sharpening in the population response profile could theoretically improve the probability of correctly discriminating high-value stimuli from low-value alternatives. Footnotes Copyright © 2010 The American Physiological Society

Zhang, Min-Min; Gruszczynski, Pawel; Walewska, Aleksandra; Bulaj, Grzegorz; Olivera, Baldomero M.; Yoshikami, Doju

doi: 10.1152/jn.00145.2010pmid: 20410356

Abstract The guanidinium alkaloids tetrodotoxin (TTX) and saxitoxin (STX) are classic ligands of voltage-gated sodium channels (VGSCs). Like TTX and STX, μ-conotoxin peptides are pore blockers but with greater VGSC subtype selectivity. μ-Conotoxin KIIIA blocks the neuronal subtype Na V 1.2 with nanomolar affinity and we recently discovered that KIIIA and its mutant with one fewer positive charge, KIIIAK7A, could act synergistically with TTX in a ternary peptide·TTX·Na V complex. In the complex, the peptide appeared to trap TTX in its normal binding site such that TTX could not readily dissociate from the channel until the peptide had done so; in turn, the presence of TTX accelerated the rate at which peptide dissociated from the channel. In the present study we examined the inhibition of Na V 1.2, exogenously expressed in Xenopus oocytes, by STX (a divalent cation) and its sulfated congener GTX2/3 (with a net +1 charge). Each could form a ternary complex with KIIIA and Na V 1.2, as previously found with TTX (a monovalent cation), but only when STX or GTX2/3 was added before KIIIA. The KIIIA·alkaloid·Na V complex was considerably less stable with STX than with either GTX2/3 or TTX. In contrast, ternary KIIIAK7A·alkaloid·Na V complexes could be formed with either order of ligand addition and were about equally stable with STX, GTX2/3, or TTX. The most parsimonious interpretation of the overall results is that the alkaloid and peptide are closely apposed in the ternary complex. The demonstration that two interacting ligands (“syntoxins”) occupy adjacent sites raises the possibility of evolving a much more sophisticated neuropharmacology of VGSCs. Copyright © 2010 The American Physiological Society

Popescu, Maria V.; Ebner, Ford F.

doi: 10.1152/jn.00120.2009pmid: 20427621

Abstract The normal development of sensory perception in mammals depends on appropriate sensory experience between birth and maturity. Numerous reports have shown that trimming some or all of the large mystacial vibrissa (whiskers) on one side of the face after birth has a detrimental effect on the maturation of cortical function. The objective of the present study was to understand the differences that occur after unilateral whisker trimming compared with those that occur after bilateral deprivation. Physiological deficits produced by bilateral trimming (BD) of all whiskers for 2 mo after birth were compared with the deficits produced by unilateral trimming (UD) for the same period of time using extracellular recording under urethan anesthesia from single cells in rat barrel cortex. Fast spiking (FSUs) and regular spiking (RSUs) units were separated and their properties compared in four subregions identified by histological reconstructions of the electrode penetrations, namely: layer IV barrel and septum, and layers II/III above a barrel and above a septum. UD upregulated responses in layer IV septa and in layers II/III above septa and perturbed the timing of responses to whisker stimuli. After BD, nearly all responses were decreased, and poststimulus latencies were increased. Circuit changes are proposed as an argument for how inputs arising from the spared whiskers project to the undeprived cortex and, via commissural fibers, could upregulate septal responses after UD. Following BD, more global neural deficits create a signature difference in the outcome of UD and BD in rat barrel cortex. Footnotes Copyright © 2010 The American Physiological Society

Netser, Shai; Ohayon, Shay; Gutfreund, Yoram

doi: 10.1152/jn.01142.2009pmid: 20427617

Abstract It is well established that the optic tectum (or its mammalian homologue, the superior colliculus) is involved in directing gaze toward salient stimuli. However, salient stimuli typically induce orienting responses beyond gaze shifts. The role of the optic tectum in generating responses such as pupil dilation, galvanic responses, or covert shifts is not clear. In the present work, we studied the effects of microstimulation in the optic tectum of the barn owl ( Tyto alba ) on pupil diameter and on eye shifts. Experiments were conducted in lightly anesthetized head-restrained barn owls. We report that low-level microstimulation in the deep layers of the optic tectum readily induced pupil dilation responses (PDRs), as well as small eye movements. Electrically evoked PDRs, similar to acoustically evoked PDRs, were long-lasting and habituated to repeated stimuli. We further show that microstimulation in the external nucleus of the inferior colliculus also induced PDRs. Finally, in experiments in which tectal microstimulations were coupled with acoustic stimuli, we show a tendency of the microstimulation to enhance pupil responses and eye shifts to previously habituated acoustic stimuli. The enhancement was dependent on the site of stimulation in the tectal spatial map; responses to sounds with spatial cues that matched the site of stimulation were more enhanced compared with sounds with spatial cues that did not match. These results suggest that the optic tectum is directly involved in autonomic orienting reflexes as well as in gaze shifts, highlighting the central role of the optic tectum in mediating the body responses to salient stimuli. Footnotes Copyright © 2010 The American Physiological Society