Showing papers on "Receptive field published in 2010"

Dendritic organization of sensory input to cortical neurons in vivo

Abstract: In sensory cortex regions, neurons are tuned to specific stimulus features. For example, in the visual cortex, many neurons fire predominantly in response to moving objects of a preferred orientation. However, the characteristics of the synaptic input that cortical neurons receive to generate their output firing pattern remain unclear. Here we report a novel approach for the visualization and functional mapping of sensory inputs to the dendrites of cortical neurons in vivo. By combining high-speed two-photon imaging with electrophysiological recordings, we identify local subthreshold calcium signals that correspond to orientation-specific synaptic inputs. We find that even inputs that share the same orientation preference are widely distributed throughout the dendritic tree. At the same time, inputs of different orientation preference are interspersed, so that adjacent dendritic segments are tuned to distinct orientations. Thus, orientation-tuned neurons can compute their characteristic firing pattern by integrating spatially distributed synaptic inputs coding for multiple stimulus orientations.

Fly Motion Vision

Abstract: Fly motion vision and resultant compensatory optomotor responses are a classic example for neural computation. Here we review our current understanding of processing of optic flow as generated by an animal's self-motion. Optic flow processing is accomplished in a series of steps: First, the time-varying photoreceptor signals are fed into a two-dimensional array of Reichardt-type elementary motion detectors (EMDs). EMDs compute, in parallel, local motion vectors at each sampling point in space. Second, the output signals of many EMDs are spatially integrated on the dendrites of large-field tangential cells in the lobula plate. In the third step, tangential cells form extensive interactions with each other, giving rise to their large and complex receptive fields. Thus, tangential cells can act as matched filters tuned to optic flow during particular flight maneuvers. They finally distribute their information onto postsynaptic descending neurons, which either instruct the motor centers of the thoracic ganglion for flight and locomotion control or act themselves as motor neurons that control neck muscles for head movements.

Developmental sensory experience balances cortical excitation and inhibition

Abstract: Early in life, neural circuits are highly susceptible to outside influences. The organization of the primary auditory cortex (A1) in particular is governed by acoustic experience during the critical period, an epoch near the beginning of postnatal development throughout which cortical synapses and networks are especially plastic. This neonatal sensitivity to the pattern of sensory inputs is believed to be essential for constructing stable and adequately adapted representations of the auditory world and for the acquisition of language skills by children. One important principle of synaptic organization in mature brains is the balance between excitation and inhibition, which controls receptive field structure and spatiotemporal flow of neural activity, but it is unknown how and when this excitatory-inhibitory balance is initially established and calibrated. Here we use whole-cell recording to determine the processes underlying the development of synaptic receptive fields in rat A1. We find that, immediately after the onset of hearing, sensory-evoked excitatory and inhibitory responses are equally strong, although inhibition is less stimulus-selective and mismatched with excitation. However, during the third week of postnatal development, excitation and inhibition become highly correlated. Patterned sensory stimulation drives coordinated synaptic changes across receptive fields, rapidly improves excitatory-inhibitory coupling and prevents further exposure-induced modifications. Thus, the pace of cortical synaptic receptive field development is set by progressive, experience-dependent refinement of intracortical inhibition.

Distinct superficial and deep laminar domains of activity in the visual cortex during rest and stimulation.

Abstract: Spatial patterns of spontaneous neural activity at rest have previously been associated with specific networks in the brain, including those pertaining to the functional architecture of the primary visual cortex (V1). However, despite the prominent anatomical differences between cortical layers, little is known about the laminar pattern of spontaneous activity in V1. We address this topic by investigating the amplitude and coherence of ongoing local field potential (LFP) signals measured from different layers in V1 of macaque monkeys during rest and upon presentation of a visual stimulus. We used a linear microelectrode array to measure LFP signals at multiple, evenly spaced positions throughout the cortical thickness. Analyzing both the mean LFP amplitudes and between-contact LFP coherences, we identified two distinct zones of activity, roughly corresponding to superficial and deep layers, divided by a sharp transition near the bottom of layer 4. The LFP signals within each laminar zone were highly coherent, whereas those between zones were not. This functional compartmentalization was found not only during rest, but also when the receptive field was stimulated during a visual task. These results demonstrate the existence of distinct superficial and deep functional domains of coherent LFP activity in V1 that may reflect the intrinsic interplay of V1 microcircuitry with cortical and subcortical targets, respectively.

Parallel processing of visual space by neighboring neurons in mouse visual cortex

Abstract: Visual cortex exhibits smooth retinotopic organization on the macroscopic scale, but it is unknown how receptive fields are organized at the level of neighboring neurons. This information is crucial for discriminating among models of visual cortex. We used in vivo two-photon calcium imaging to independently map ON and OFF receptive field subregions of local populations of layer 2/3 neurons in mouse visual cortex. We found that receptive field subregions are often precisely shared among multiple neighboring neurons. Furthermore, large subregions appear to be assembled from multiple smaller, non-overlapping subregions of other neurons in the same local population. These experiments provide the first characterization of the diversity of receptive fields in a dense local network of visual cortex, and reveal elementary units of receptive field organization. Our results suggest that a limited pool of afferent receptive fields is available to a local population of neurons, and reveal new organizational principles for the neural circuitry of the mouse visual cortex.

Visual Representations by Cortical Somatostatin Inhibitory Neurons—Selective But with Weak and Delayed Responses

Abstract: Somatostatin-expressing inhibitory (SOM) neurons in the sensory cortex consist mostly of Martinotti cells, which project ascending axons to layer 1. Due to their sparse distribution, the representational properties of these neurons remain largely unknown. By two-photon imaging guided cell-attached recordings, we characterized visual response and receptive field (RF) properties of SOM neurons and parvalbumin-expressing inhibitory (PV) neurons genetically labeled in the mouse primary visual cortex. In contrast to PV neurons, SOM neurons exhibit broader spikes, lower spontaneous firing rates, smaller On/Off subfields, and broader ranges of basic RF properties such as On/Off segregation, orientation and direction tunings. Notably, the level of orientation and direction selectivity is comparable to that of excitatory neurons, from weakly-tuned to highly selective, whereas PV neurons are in general unselective. Strikingly, the evoked spiking responses of SOM cells are ∼3- to 5-fold weaker and 20-25 ms delayed compared with those of PV neurons. The onset latency of the latter is consistent with that of inhibitory input to excitatory neurons. These functional differences between SOM and PV neurons exist in both layer 2/3 and 4. Our results suggest that SOM and PV neurons engage in cortical circuits in different manners: while PV neurons provide fast, strong but untuned feedforward inhibition to excitatory neurons, likely serving as a general gain control for the processing of ascending inputs, SOM neurons with their selective but delayed and weak inhibition may provide more specific gating of later arriving intracortical excitatory inputs on the distal dendrites.

Visual Receptive Field Properties of Neurons in the Superficial Superior Colliculus of the Mouse

Abstract: The mouse is a promising model in the study of visual system function and development because of available genetic tools. However, a quantitative analysis of visual receptive field properties had not been performed in the mouse superior colliculus (SC) despite its importance in mouse vision and its usefulness in developmental studies. We have made single-unit extracellular recordings from superficial layers of the SC in urethane-anesthetized C57BL/6 mice. We first map receptive fields with flashing spot stimuli and show that most SC neurons have spatially overlapped ON and OFF subfields. With drifting sinusoidal gratings, we then determine the tuning properties of individual SC neurons, including selectivity for stimulus direction and orientation, spatial frequency tuning, temporal frequency tuning, response linearity, and size preference. A wide range of receptive field sizes and selectivity are observed across the population and in various subtypes of SC neurons identified morphologically. In particular, orientation-selective responses are discovered in the mouse SC, and they are not affected by cortical lesion or long-term visual deprivation. However, ON/OFF characteristics and spatial frequency tuning of SC neurons are influenced by cortical inputs and require visual experience during development. Together, our results provide essential information for future investigations on the functional development of the superior colliculus.

Fine-Tuning of Pre-Balanced Excitation and Inhibition During Auditory Cortical Development

Abstract: In order to build a proper and stable representation of the auditory world, neonatal rodents exhibit a significant degree of circuit plasticity, allowing for sensitivity to the pattern of sensory inputs. During this time, neurons construct a receptive field, one that relies upon a particular balance of excitatory and inhibitory inputs, yet it is unknown as to how this balance is formed. Two studies published in this issue of Nature reveal contrasting views as to how the mature system develops. Excitation and inhibition were found to be equally strong upon hearing onset in each study. But whereas Dorrn et al. find evidence for an experience-dependent refinement of inhibition as the receptive fields develop, Sun et al. observed a fine adjustment in the excitatory input strength to produce a shifted balance. Nevertheless, taken together, both studies point towards a fine adjustment of synaptic inputs as the force behind the production of mature receptive fields, as opposed to more radical changes such as input pruning. To build a representation of the auditory world, neuronal circuits in neonatal rodents exhibit plasticity, allowing sensitivity to the pattern of sensory inputs. At this time, neurons construct a receptive field, which relies on a balance of excitatory and inhibitory inputs. Here, excitation and inhibition were found to be co-tuned upon hearing onset, but later an adjustment in the excitatory input strength occurred. Thus a fine adjustment in synaptic inputs, rather than more radical changes such as input pruning, may refine mature receptive fields. Functional receptive fields of neurons in sensory cortices undergo progressive refinement during development1,2,3,4. Such refinement may be attributed to the pruning of non-optimal excitatory inputs, reshaping of the excitatory tuning profile through modifying the strengths of individual inputs, or strengthening of cortical inhibition. These models have not been directly tested because of the technical difficulties in assaying the spatiotemporal patterns of functional synaptic inputs during development. Here we apply in vivo whole-cell voltage-clamp recordings to the recipient layer 4 neurons in the rat primary auditory cortex (A1) to determine the developmental changes in the frequency–intensity tonal receptive fields (TRFs) of their excitatory and inhibitory inputs. Surprisingly, we observe co-tuned excitation and inhibition immediately after the onset of hearing, suggesting that a tripartite thalamocortical circuit with relatively strong feedforward inhibition is formed independently of auditory experience. The frequency ranges of tone-driven excitatory and inhibitory inputs first expand within a few days of the onset of hearing and then persist into adulthood. The latter phase is accompanied by a sharpening of the excitatory but not inhibitory frequency tuning profile, which results in relatively broader inhibitory tuning in adult A1 neurons. Thus the development of cortical synaptic TRFs after the onset of hearing is marked by a slight breakdown of previously formed excitation–inhibition balance. Our results suggest that functional refinement of cortical TRFs does not require a selective pruning of inputs, but may depend more on a fine adjustment of excitatory input strengths.

Shared mapping of own and others' bodies in visuotactile bimodal area of monkey parietal cortex

Abstract: Parietal cortex contributes to body representations by integrating visual and somatosensory inputs. Because mirror neurons in ventral premotor and parietal cortices represent visual images of others' actions on the intrinsic motor representation of the self, this matching system may play important roles in recognizing actions performed by others. However, where and how the brain represents others' bodies and correlates self and other body representations remain unclear. We expected that a population of visuotactile neurons in simian parietal cortex would represent not only own but others' body parts. We first searched for parietal visuotactile bimodal neurons in the ventral intraparietal area and area 7b of monkeys, and then examined the activity of these neurons while monkeys were observing visual or tactile stimuli placed on the experimenter's body parts. Some bimodal neurons with receptive fields (RFs) anchored on the monkey's body exhibited visual responses matched to corresponding body parts of the experimenter, and visual RFs near that body part existed in the peripersonal space within approximately 30 cm from the body surface. These findings suggest that the brain could use self representation as a reference for perception of others' body parts in parietal cortex. These neurons may contribute to spatial matching between the bodies of the self and others in both action recognition and imitation.

Six different roles for crossover inhibition in the retina: Correcting the nonlinearities of synaptic transmission

Abstract: Early retinal studies categorized ganglion cell behavior as either linear or nonlinear and rectifying as represented by the familiar X- and Y-type ganglion cells in cat. Nonlinear behavior is in large part a consequence of the rectifying nonlinearities inherent in synaptic transmission. These nonlinear signals underlie many special functions in retinal processing, including motion detection, motion in motion, and local edge detection. But linear behavior is also required for some visual processing tasks. For these tasks, the inherently nonlinear signals are "linearized" by "crossover inhibition." Linearization utilizes a circuitry whereby nonlinear ON inhibition adds with nonlinear OFF excitation or ON excitation adds with OFF inhibition to generate a more linear postsynaptic voltage response. Crossover inhibition has now been measured in most bipolar, amacrine, and ganglion cells. Functionally crossover inhibition enhances edge detection, allows ganglion cells to recognize luminance-neutral patterns with their receptive fields, permits ganglion cells to distinguish contrast from luminance, and maintains a more constant conductance during the light response. In some cases, crossover extends the operating range of cone-driven OFF ganglion cells into the scotopic levels. Crossover inhibition is also found in neurons of the lateral geniculate nucleus and V1.

Receptive-field properties of V1 and V2 neurons in mice and macaque monkeys.

Abstract: We report the results of extracellular single-unit recording experiments where we quantitatively analyzed the receptive-field (RF) properties of neurons in V1 and an adjacent extrastriate visual area (V2L) of anesthetized mice with emphasis on the RF center-surround organization. We compared the results with the RF center-surround organization of V1 and V2 neurons in macaque monkeys. If species differences in spatial scale are taken into consideration, mouse V1 and V2L neurons had remarkably fine stimulus selectivity, and the majority of response properties in V2L were not different from those in V1. The RF center-surround organization of mouse V1 neurons was qualitatively similar to that for macaque monkeys (i.e., the RF center is surrounded by extended suppressive regions). However, unlike in monkey V2, a significant proportion of cortical neurons, largely complex cells in V2L, did not exhibit quantifiable RF surround suppression. Simple cells had smaller RF centers than complex cells, and the prevalence and strength of surround suppression were greater in simple cells than in complex cells. These findings, particularly on the RF center-surround organization of visual cortical neurons, give new insights into the principles governing cortical circuits in the mouse visual cortex and should provide further impetus for the use of mice in studies on the genetic and molecular basis of RF development and synaptic plasticity.

Intervening inhibition underlies simple-cell receptive field structure in visual cortex

Abstract: Synaptic inputs underlying spike receptive fields are important for understanding mechanisms of neuronal processing. Using whole-cell voltage-clamp recordings from neurons in mouse primary visual cortex, we examined the spatial patterns of their excitatory and inhibitory synaptic inputs evoked by On and Off stimuli. Neurons with either segregated or overlapped On/Off spike subfields had substantial overlaps between all the four synaptic subfields. The segregated receptive-field structures were generated by the integration of excitation and inhibition with a stereotypic 'overlap-but-mismatched' pattern: the peaks of excitatory On/Off subfields were separated and flanked colocalized peaks of inhibitory On/Off subfields. The small mismatch of excitation/inhibition led to an asymmetric inhibitory shaping of On/Off spatial tunings, resulting in a great enhancement of their distinctiveness. Thus, slightly separated On/Off excitation, together with intervening inhibition, can create simple-cell receptive-field structure and the dichotomy of receptive-field structures may arise from a fine-tuning of the spatial arrangement of synaptic inputs.

Analysis of the context integration mechanisms underlying figure-ground organization in the visual cortex

Abstract: Most neurons in visual cortex respond to contrast borders and are orientation selective, and some are also selective for which side of a border is figure and which side is ground ("border ownership coding"). These neurons are influenced by the image context far beyond the classical receptive field (CRF) and as early as 25 ms after the onset of activity in the cortex. The nature of the fast context integration mechanism is not well understood. What parts of a figure contribute to the context effect? What is the structure of the "extraclassical surround"? Is the context information propagated through horizontal fibers within cortex or through reciprocal connections via higher-level areas? To address these questions, we studied border ownership modulation with fragmented figures. Neurons were recorded in areas V1 and V2 of Macaca mulatta under behaviorally induced fixation. Test figures were fragmented rectangles. While one edge was centered on the CRF, the presence of the fragments outside the CRF was varied. The surround fragments produced facilitation on the preferred border ownership side as well as suppression on the nonpreferred side, with approximately 80% of the locations contributing on average. Fragments far from the CRF influenced the responses even in the absence of fragments closer to the CRF, and without the extra delay that would incur from propagation through horizontal fibers. Three principally different models are discussed. The results support a model in which the antagonistic surround influences are produced by reentrant signals from a higher-level area.

Encoding of whisker input by cerebellar Purkinje cells

Abstract: The cerebellar cortex is crucial for sensorimotor integration Sensorimotor inputs converge on cerebellar Purkinje cells via two afferent pathways: the climbing fibre pathway triggering complex spikes, and the mossy fibre–parallel fibre pathway, modulating the simple spike activities of Purkinje cells We used, for the first time, the mouse whisker system as a model system to study the encoding of somatosensory input by Purkinje cells We show that most Purkinje cells in ipsilateral crus 1 and crus 2 of awake mice respond to whisker stimulation with complex spike and/or simple spike responses Single-whisker stimulation in anaesthetised mice revealed that the receptive fields of complex spike and simple spike responses were strikingly different Complex spike responses, which proved to be sensitive to the amplitude, speed and direction of whisker movement, were evoked by only one or a few whiskers Simple spike responses, which were not affected by the direction of movement, could be evoked by many individual whiskers The receptive fields of Purkinje cells were largely intermingled, and we suggest that this facilitates the rapid integration of sensory inputs from different sources Furthermore, we describe that individual Purkinje cells, at least under anaesthesia, may be bound in two functional ensembles based on the receptive fields and the synchrony of the complex spike and simple spike responses The ‘complex spike ensembles’ were oriented in the sagittal plane, following the anatomical organization of the climbing fibres, while the ‘simple spike ensembles’ were oriented in the transversal plane, as are the beams of parallel fibres

Global Inhibition and Stimulus Competition in the Owl Optic Tectum

Abstract: Stimulus selection for gaze and spatial attention involves competition among stimuli across sensory modalities and across all of space. We demonstrate that such cross-modal, global competition takes place in the intermediate and deep layers of the optic tectum, a structure known to be involved in gaze control and attention. A variety of either visual or auditory stimuli located anywhere outside of a neuron's receptive field (RF) were shown to suppress or completely eliminate responses to a visual stimulus located inside the RF in nitrous oxide sedated owls. The essential mechanism underlying this stimulus competition is global, divisive inhibition. Unlike the effect of the classical inhibitory surround, which decreases with distance from the RF center and shapes neuronal responses to individual stimuli, global inhibition acts across the entirety of space and modulates responses primarily in the context of multiple stimuli. Whereas the source of this global inhibition is as yet unknown, our data indicate that different networks mediate the classical surround and global inhibition. We hypothesize that this global, cross-modal inhibition, which acts automatically in a bottom-up manner even in sedated animals, is critical to the creation of a map of stimulus salience in the optic tectum.

Columnar Connectivity and Laminar Processing in Cat Primary Auditory Cortex

Abstract: Author(s): Atencio, Craig A; Schreiner, Christoph E | Abstract: BackgroundRadial intra- and interlaminar connections form a basic microcircuit in primary auditory cortex (AI) that extracts acoustic information and distributes it to cortical and subcortical networks. Though the structure of this microcircuit is known, we do not know how the functional connectivity between layers relates to laminar processing.Methodology/principal findingsWe studied the relationships between functional connectivity and receptive field properties in this columnar microcircuit by simultaneously recording from single neurons in cat AI in response to broadband dynamic moving ripple stimuli. We used spectrotemporal receptive fields (STRFs) to estimate the relationship between receptive field parameters and the functional connectivity between pairs of neurons. Interlaminar connectivity obtained through cross-covariance analysis reflected a consistent pattern of information flow from thalamic input layers to cortical output layers. Connection strength and STRF similarity were greatest for intralaminar neuron pairs and in supragranular layers and weaker for interlaminar projections. Interlaminar connection strength co-varied with several STRF parameters: feature selectivity, phase locking to the stimulus envelope, best temporal modulation frequency, and best spectral modulation frequency. Connectivity properties and receptive field relationships differed for vertical and horizontal connections.Conclusions/significanceThus, the mode of local processing in supragranular layers differs from that in infragranular layers. Therefore, specific connectivity patterns in the auditory cortex shape the flow of information and constrain how spectrotemporal processing transformations progress in the canonical columnar auditory microcircuit.

Neural Ensemble Codes for Stimulus Periodicity in Auditory Cortex

Abstract: We measured the responses of neurons in auditory cortex of male and female ferrets to artificial vowels of varying fundamental frequency (f(0)), or periodicity, and compared these with the performance of animals trained to discriminate the periodicity of these sounds. Sensitivity to f(0) was found in all five auditory cortical fields examined, with most of those neurons exhibiting either low-pass or high-pass response functions. Only rarely was the stimulus dependence of individual neuron discharges sufficient to account for the discrimination performance of the ferrets. In contrast, when analyzed with a simple classifier, responses of small ensembles, comprising 3-61 simultaneously recorded neurons, often discriminated periodicity changes as well as the animals did. We examined four potential strategies for decoding ensemble responses: spike counts, relative first-spike latencies, a binary "spike or no-spike" code, and a spike-order code. All four codes represented stimulus periodicity effectively, and, surprisingly, the spike count and relative latency codes enabled an equally rapid readout, within 75 ms of stimulus onset. Thus, relative latency codes do not necessarily facilitate faster discrimination judgments. A joint spike count plus relative latency code was more informative than either code alone, indicating that the information captured by each measure was not wholly redundant. The responses of neural ensembles, but not of single neurons, reliably encoded f(0) changes even when stimulus intensity was varied randomly over a 20 dB range. Because trained animals can discriminate stimulus periodicity across different sound levels, this implies that ensemble codes are better suited to account for behavioral performance.

The Functional Properties of Barrel Cortex Neurons Projecting to the Primary Motor Cortex

Abstract: Nearby neurons, sharing the same locations within the mouse whisker map, can have dramatically distinct response properties. To understand the significance of this diversity, we studied the relationship between the responses of individual neurons and their projection targets in the mouse barrel cortex. Neurons projecting to primary motor cortex (MI) or secondary somatosensory area (SII) were labeled with red fluorescent protein (RFP) using retrograde viral infection. We used in vivo two-photon Ca(2+) imaging to map the responses of RFP-positive and neighboring L2/3 neurons to whisker deflections. Neurons projecting to MI displayed larger receptive fields compared with other neurons, including those projecting to SII. Our findings support the view that intermingled neurons in primary sensory areas send specific stimulus features to different parts of the brain.

Blue-Yellow Opponency in Primate S Cone Photoreceptors

Abstract: The neural coding of human color vision begins in the retina. The outputs of long (L)-, middle (M)-, and short (S)-wavelength-sensitive cone photoreceptors combine antagonistically to produce "red-green" and "blue-yellow" spectrally opponent signals (Hering, 1878; Hurvich and Jameson, 1957). Spectral opponency is well established in primate retinal ganglion cells (Reid and Shapley, 1992; Dacey and Lee, 1994; Dacey et al., 1996), but the retinal circuitry creating the opponency remains uncertain. Here we find, from whole-cell recordings of photoreceptors in macaque monkey, that "blue-yellow" opponency is already present in the center-surround receptive fields of S cones. The inward current evoked by blue light derives from phototransduction within the outer segment of the S cone. The outward current evoked by yellow light is caused by feedback from horizontal cells that are driven by surrounding L and M cones. Stimulation of the surround modulates calcium conductance in the center S cone.

Attentional Modulation of MT Neurons with Single or Multiple Stimuli in Their Receptive Fields

Abstract: Descriptions of how attention modulates neuronal responses suggest that the strength of its effects depends on stimulus conditions. Attention to an isolated stimulus in the receptive field of an individual neuron typically produces a moderate enhancement of the cell's response, but neuronal responses are often strongly modulated when attention is shifted between multiple stimuli that lie within the receptive field. However, previous reports have not compared these stimulus effects under equivalent conditions, so differences in task difficulty could have been responsible for much of the difference. Consequently, the quantitative effects of stimulus conditions have remained unknown, and it has not been possible to address the question of whether the differences that have been observed could be explained by a single mechanism. We measured the attentional modulation of the responses of 70 single neurons in area MT of two rhesus monkeys using a task designed to keep attention stable across different stimulus configurations. We found that attentional modulation was indeed much stronger when more than one stimulus was within the receptive field. Nevertheless, the broad range of attentional modulations seen across the different conditions could be readily explained by single mechanism. The neurophysiological data from all stimulus conditions were well fit by a model in which attention acts via a response normalization mechanism (Lee and Maunsell, 2009). Collectively, these results validate previous impressions of the effects of stimulus configuration on attentional modulation, and add support to hypothesis that attention modulation depends on a response normalization mechanism.

Laminar diversity of dynamic sound processing in cat primary auditory cortex.

Abstract: For primary auditory cortex (AI) laminae, there is little evidence of functional specificity despite clearly expressed cellular and connectional differences. Natural sounds are dominated by dynamic temporal and spectral modulations and we used these properties to evaluate local functional differences or constancies across laminae. To examine the layer-specific processing of acoustic modulation information, we simultaneously recorded from multiple AI laminae in the anesthetized cat. Neurons were challenged with dynamic moving ripple stimuli and we subsequently computed spectrotemporal receptive fields (STRFs). From the STRFs, temporal and spectral modulation transfer functions (tMTFs, sMTFs) were calculated and compared across layers. Temporal and spectral modulation properties often differed between layers. On average, layer II/III and VI neurons responded to lower temporal modulations than those in layer IV. tMTFs were mainly band-pass in granular layer IV and became more low-pass in infragranular layers. Compared with layer IV, spectral MTFs were broader and their upper cutoff frequencies higher in layers V and VI. In individual penetrations, temporal modulation preference was similar across layers for roughly 70% of the penetrations, suggesting a common, columnar functional characteristic. By contrast, only about 30% of penetrations showed consistent spectral modulation preferences across layers, indicative of functional laminar diversity or specialization. Since local laminar differences in stimulus preference do not always parallel the main flow of information in the columnar cortical microcircuit, this indicates the influence of additional horizontal or thalamocortical inputs. AI layers that express differing modulation properties may serve distinct roles in the extraction of dynamic sound information, with the differing information specific to the targeted stations of each layer.

Spatial and temporal frequency tuning in striate cortex: functional uniformity and specializations related to receptive field eccentricity.

Abstract: In light of anatomical evidence suggesting differential connection patterns in central vs. peripheral representations of cortical areas, we investigated the extent to which the response properties of cells in the primary visual area (V1) of the marmoset change as a function of eccentricity. Responses to combinations of the spatial and temporal frequencies of visual stimuli were quantified for neurons with receptive fields ranging from 3 degrees to 70 degrees eccentricity. Optimal spatial frequencies and stimulus speeds reflected the expectation that the responses of cells throughout V1 are essentially uniform, once scaled according to the cortical magnification factor. In addition, temporal frequency tuning was similar throughout V1. However, spatial frequency tuning curves depended both on the cell's optimal spatial frequency and on the receptive field eccentricity: cells with peripheral receptive fields showed narrower bandwidths than cells with central receptive fields that were sensitive to the same optimal spatial frequency. Although most V1 cells had separable spatial and temporal frequency tuning, the proportion of neurons displaying significant spatiotemporal interactions increased in the representation of far peripheral vision (> 50 degrees). In addition, of the fewer than 5% of V1 cells that showed robust (spatial frequency independent) selectivity to stimulus speed, most were concentrated in the representation of the far periphery. Spatiotemporal interactions in the responses of many cells in the peripheral representation of V1 reduced the ambiguity of responses to high-speed (> 30 degrees/s) signals. These results support the notion of a relative specialization for motion processing in the far peripheral representations of cortical areas, including V1.

Discrimination of Communication Vocalizations by Single Neurons and Groups of Neurons in the Auditory Midbrain

Abstract: Many social animals including songbirds use communication vocalizations for individual recognition. The perception of vocalizations depends on the encoding of complex sounds by neurons in the ascending auditory system, each of which is tuned to a particular subset of acoustic features. Here, we examined how well the responses of single auditory neurons could be used to discriminate among bird songs and we compared discriminability to spectrotemporal tuning. We then used biologically realistic models of pooled neural responses to test whether the responses of groups of neurons discriminated among songs better than the responses of single neurons and whether discrimination by groups of neurons was related to spectrotemporal tuning and trial-to-trial response variability. The responses of single auditory midbrain neurons could be used to discriminate among vocalizations with a wide range of abilities, ranging from chance to 100%. The ability to discriminate among songs using single neuron responses was not correlated with spectrotemporal tuning. Pooling the responses of pairs of neurons generally led to better discrimination than the average of the two inputs and the most discriminating input. Pooling the responses of three to five single neurons continued to improve neural discrimination. The increase in discriminability was largest for groups of neurons with similar spectrotemporal tuning. Further, we found that groups of neurons with correlated spike trains achieved the largest gains in discriminability. We simulated neurons with varying levels of temporal precision and measured the discriminability of responses from single simulated neurons and groups of simulated neurons. Simulated neurons with biologically observed levels of temporal precision benefited more from pooling correlated inputs than did neurons with highly precise or imprecise spike trains. These findings suggest that pooling correlated neural responses with the levels of precision observed in the auditory midbrain increases neural discrimination of complex vocalizations.

Spectral and Temporal Modulation Tradeoff in the Inferior Colliculus

Abstract: The cochlea encodes sounds through frequency-selective channels that exhibit low-pass modulation sensitivity. Unlike the cochlea, neurons in the auditory midbrain are tuned for spectral and temporal modulations found in natural sounds, yet the role of this transformation is not known. We report a distinct tradeoff in modulation sensitivity and tuning that is topographically ordered within the central nucleus of the inferior colliculus (CNIC). Spectrotemporal receptive fields (STRFs) were obtained with 16-channel electrodes inserted orthogonal to the isofrequency lamina. Surprisingly, temporal and spectral characteristics exhibited an opposing relationship along the tonotopic axis. For low best frequencies (BFs), units were selective for fast temporal and broad spectral modulations. A systematic progression was observed toward slower temporal and finer spectral modulation sensitivity at high BF. This tradeoff was strongly reflected in the arrangement of excitation and inhibition and, consequently, in the modulation tuning characteristics. Comparisons with auditory nerve fibers show that these trends oppose the pattern imposed by the peripheral filters. These results suggest that spectrotemporal preferences are reordered within the tonotopic axis of the CNIC. This topographic organization has profound implications for the coding of spectrotemporal features in natural sounds and could underlie a number of perceptual phenomena.

Symmetry Breakdown in the ON and OFF Pathways of the Retina at Night: Functional Implications

Abstract: Several recent studies have shown that the ON and OFF channels of the visual system are not simple mirror images of each other, that their response characteristics are asymmetric (Chichilnisky and Kalmar, 2002; Sagdullaev and McCall, 2005). How the asymmetries bear on visual processing is not well understood. Here, we show that ON and OFF ganglion cells show a strong asymmetry in their temporal adaptation to photopic (day) and scotopic (night) conditions and that the asymmetry confers a functional advantage. Under photopic conditions, the ON and OFF ganglion cells show similar temporal characteristics. Under scotopic conditions, the two cell classes diverge—ON cells shift their tuning to low temporal frequencies, whereas OFF cells continue to respond to high. This difference in processing corresponds to an asymmetry in the natural world, one produced by the Poisson nature of photon capture and persists over a broad range of light levels. This work characterizes a previously unknown divergence in the ON and OFF pathways and its utility to visual processing. Furthermore, the results have implications for downstream circuitry and thus offer new constraints for models of downstream processing, since ganglion cells serve as building blocks for circuits in higher brain areas. For example, if simple cells in visual cortex rely on complementary interactions between the two pathways, such as push–pull interactions (Alonso et al., 2001; Hirsch, 2003), their receptive fields may be radically different under scotopic conditions, when the ON and OFF pathways are out of sync.

Spike Timing and Information Transmission at Retinogeniculate Synapses

Abstract: This study examines the rules governing the transfer of spikes between the retina and the lateral geniculate nucleus (LGN) with the goal of determining whether the most informative retinal spikes preferentially drive LGN responses and what role spike timing plays in the process. By recording from monosynaptically connected pairs of retinal ganglion cells and LGN neurons in vivo in the cat, we show that relayed spikes are more likely than nonrelayed spikes to be evoked by stimuli that match the receptive fields of the recorded cells and that an interspike interval-based mechanism contributes to the process. Relayed spikes are also more reliable in their timing and number where they often achieve the theoretical limit of minimum variance. As a result, relayed spikes carry more visual information per spike. Based on these results, we conclude that retinogeniculate processing increases sparseness in the neural code by selectively relaying the highest fidelity spikes to the visual cortex.