Comparison of LFP-based and spike-based spectro-temporal receptive fields and cross-correlation in cat primary auditory cortex

Multi-electrode array recordings of spike and local field potential (LFP) activity were made from primary auditory cortex of 12 normal hearing, ketamine-anesthetized cats. We evaluated 259 spectro-temporal receptive fields (STRFs) and 492 frequency-tuning curves (FTCs) based on LFPs and spikes simultaneously recorded on the same electrode. We compared their characteristic frequency (CF) gradients and their cross-correlation distances. The CF gradient for spike-based FTCs was about twice that for 2-40 Hz-filtered LFP-based FTCs, indicating greatly reduced frequency selectivity for LFPs. We also present comparisons for LFPs band-pass filtered between 4-8 Hz, 8-16 Hz and 16-40 Hz, with spike-based STRFs, on the basis of their marginal frequency distributions. We find on average a significantly larger correlation between the spike based marginal frequency distributions and those based on the 16-40 Hz filtered LFP, compared to those based on the 4-8 Hz, 8-16 Hz and 2-40 Hz filtered LFP. This suggests greater frequency specificity for the 16-40 Hz LFPs compared to those of lower frequency content. For spontaneous LFP and spike activity we evaluated 1373 pair correlations for pairs with >200 spikes in 900 s per electrode. Peak correlation-coefficient space constants were similar for the 2-40 Hz filtered LFP (5.5 mm) and the 16-40 Hz LFP (7.4 mm), whereas for spike-pair correlations it was about half that, at 3.2 mm. Comparing spike-pairs with 2-40 Hz (and 16-40 Hz) LFP-pair correlations showed that about 16% (9%) of the variance in the spike-pair correlations could be explained from LFP-pair correlations recorded on the same electrodes within the same electrode array. This larger correlation distance combined with the reduced CF gradient and much broader frequency selectivity suggests that LFPs are not a substitute for spike activity in primary auditory cortex.     

Multiple-band trigger features of midbrain auditory neurons revealed in composite spectro-temporal receptive fields

Receptive fields of single units in the auditory midbrain of anesthetized rats were studied using random FM-tone stimuli of narrow frequency-ranges. Peri-spike averaging of the modulating waveform first produced a spectro-temporal receptive field (STRF). Combining STRFs obtained from the same unit at different frequency regions generated a composite receptive field covering a wider frequency range of 2 to 3 octaves. About 20% of the composite STRFs (26/122) showed a pattern of multiple-bands which were not clear in the non-composite maps. Multiple-bands in a given composite map were often oriented in the same direction (representing upward or downward FM ramp) separated at rather regular frequency intervals. They reflect multiple FM trigger features in the stimulus rather than repetitive firing to a single trigger feature. Results showed that the subcortical auditory pathways are capable of detecting multiple FM features and such sensitivity could be useful in detecting multiple-harmonic FM bands present in the vocalization sounds.     

Understanding auditory spectro-temporal receptive fields and their changes with input statistics by efficient coding principles

Spectro-temporal receptive fields (STRFs) have been widely used as linear approximations to the signal transform from sound spectrograms to neural responses along the auditory pathway. Their dependence on statistical attributes of the stimuli, such as sound intensity, is usually explained by nonlinear mechanisms and models. Here, we apply an efficient coding principle which has been successfully used to understand receptive fields in early stages of visual processing, in order to provide a computational understanding of the STRFs. According to this principle, STRFs result from an optimal tradeoff between maximizing the sensory information the brain receives, and minimizing the cost of the neural activities required to represent and transmit this information. Both terms depend on the statistical properties of the sensory inputs and the noise that corrupts them. The STRFs should therefore depend on the input power spectrum and the signal-to-noise ratio, which is assumed to increase with input intensity. We analytically derive the optimal STRFs when signal and noise are approximated as Gaussians. Under the constraint that they should be spectro-temporally local, the STRFs are predicted to adapt from being band-pass to low-pass filters as the input intensity reduces, or the input correlation becomes longer range in sound frequency or time. These predictions qualitatively match physiological observations. Our prediction as to how the STRFs should be determined by the input power spectrum could readily be tested, since this spectrum depends on the stimulus ensemble. The potentials and limitations of the efficient coding principle are discussed.     

Characterizing auditory receptive fields

In this issue of Neuron, two papers by Atencio et al. and Nagel and Doupe adapt new computational methods to map the spectrotemporal response fields of neurons in the auditory cortex. The papers take different but complementary approaches to apply theoretical techniques to classical methods of receptive field mapping and, in doing so, provide exciting new insights into the way in which sounds are processed in the auditory cortex.     

A computational model of rapid task-related plasticity of auditory cortical receptive fields

Receptive field properties of neurons in A1 can rapidly adapt their shapes during task performance in accord with specific task demands and salient sensory cues (Fritz et al., Hearing Research, 206:159–176, 2005a, Nature Neuroscience, 6: 1216–1223, 2003). Such modulatory changes selectively enhance overall cortical responsiveness to target (foreground) sounds and thus increase the likelihood of detection against the background of reference sounds. In this study, we develop a mathematical model to describe how enhancing discrimination between two arbitrary classes of sounds can lead to the observed receptive field changes in a variety of spectral and temporal discrimination tasks. Cortical receptive fields are modeled as filters that change their spectro-temporal tuning properties so as to respond best to the discriminatory acoustic features between foreground and background stimuli. We also illustrate how biologically plausible constraints on the spectro-temporal tuning of the receptive fields can be used to optimize the plasticity. Results of the model simulations are compared to published data from a variety of experimental paradigms.     

Spectro-temporal receptive fields of auditory neurons in the grassfrog

The nature of the stimulus-response relation for single auditory neurons is reflected in the properties of the Pre-Event Stimulus Ensemble: the ensemble of stimuli, preceding the occurrence of an action potential (neural event). This paper describes methods to analyse the spectro-temporal properties of this ensemble. These methods are based on the analytic signal representation of acoustic signals and functionals derived from it: the instantaneous amplitude and instantaneous frequency and the dynamic power spectrum. The procedures have been applied to a number of extra-cellular single unit recordings from the grassfrog, Rana temporatia L., recorded during presentation of an ensemble of tonal stimuli. The outcome of this analysis describes the spectro-temporal receptive field of the neuron under the present stimulus conditions. The procedure, based on the dynamic power spectrum is applicable to an arbitrary stimulus ensemble, thus allowing a comparison of the spectrotemporal receptive fields for different types of stimuli.     

Spectro-temporal receptive fields of auditory neurons in the grassfrog

The stimulus-event relation of single units in the auditory midbrain area, the torus semicircularis, of the anaesthetized grassfrog (Rana temporaria L.) during stimulation with a wide ensemble of natural stimuli, was analysed using first and second order statistical analysis techniques. The average stimulus preceding the occurrence of action potentials, in general, did not prove to give very informative results. The second order procedure consisted in the determination of the average dynamic power spectrum of the pre-event stimuli, following procedures as described elsewhere (Aertsen and Johannesma, 1980; Aertsen et al., 1980). The outcome of this analysis was filtered with the overall power spectrum of the complete stimulus ensemble in order to correct for its non-uniform spectral composition. The stimulus-filtered average pre-event dynamic spectrum gives a first indication of the spectro-temporal receptive field of a neuron under natural stimulus conditions. Results for a limited number of recordings are presented and, globally, compared to the outcome of an analogous analysis of experiments with tonal stimuli.     

Binaural processing in the synthesis of auditory spatial receptive fields

The owls auditory system computes interaural time (ITD) and interaural level (ILD) differences to create a two-dimensional map of auditory space. Space-specific neurons are selective for combinations of ITD and ILD, which define, respectively, the horizontal and vertical dimensions of their receptive fields. ITD curves for postsynaptic potentials indicate that ICx neurons integrate the results of binaural cross correlation in different frequency bands. However, the difference between the main and side peaks is slight. ICx neurons further enhance this difference in the process of converting membrane potentials to impulse rates. Comparison of subthreshold postsynaptic potentials (PSPs) and spike output for the same neurons showed that receptive fields measured in PSPs were much larger than those measured in spikes in both ITD and ILD dimensions. A multiplication of separate postsynaptic potentials tuned to ITD and ILD can account for the combination sensitivity of these neurons to ITD–ILD pairs.     

Extents of visual, auditory and bimodal receptive fields of single neurons in the feline visual associative cortex

Extracellular microelectrode recordings were carried out on 150 neurons in the anterior ectosylvian sulcal region of halothane-anesthetized, immobilized, artificially ventilated cats. Fifty-nine neurons were visual, 60 were auditory and 31 were bimodal visual-auditory. As the extent of the receptive fields has never been exactly determined, we introduced a quasi-objective, computer-based, statistical method in order to estimate the receptive field sizes in the anterior half of the perimeter. The visual, auditory and bimodal cells had very large receptive fields, often with portions extending well into the ipsilateral hemifield. The mean extents of the visual and auditory receptive fields in the horizontal plane were 75.75 degrees (N=59, SD: +/- 28.620, range: 15-135 degrees), and 132.5 degrees (N=60, SD: +/- 46.72 degrees, range: 15-165 degrees) respectively. These data suggest that a single visual neuron can carry information from the whole visual field of the right eye and a single auditory unit can carry information of azimuths throughout the whole area of the horizontal plane studied. The mean extent of the bimodal receptive fields in the horizontal plane was 82.1 degrees (N=31, SD: +/- 24.24 degrees, range: 30-135 degrees). In 21 of the 31 bimodal cells we observed a facilitatory interaction between visual and auditory stimuli. The mean extent of the facilitatory interactions in these cells was 75.75 degrees (N=21, SD: +/- 24.56 degrees, range: 45-135 degrees).     

Changes in visual receptive fields with microstimulation of frontal cortex

The influence of attention on visual cortical neurons has been described in terms of its effect on the structure of receptive fields (RFs), where multiple stimuli compete to drive neural responses and ultimately behavior. We stimulated the frontal eye field (FEF) of passively fixating monkeys and produced changes in V4 responses similar to known effects of voluntary attention. Subthreshold FEF stimulation enhanced visual responses at particular locations within the RF and altered the interaction between pairs of RF stimuli to favor those aligned with the activated FEF site. Thus, we could influence which stimulus drove the responses of individual V4 neurons. These results suggest that spatial signals involved in saccade preparation are used to covertly select among multiple stimuli appearing within the RFs of visual cortical neurons.     

A model of lateral interactions as the origin of multiwhisker receptive fields in rat barrel cortex

Journal of Computational Neuroscience - While cells within barrel cortex respond primarily to deflections of their principal whisker (PW), they also exhibit responses to non-principal, or adjacent,...     

Spatio-temporal organization of receptive fields of the cat striate cortex

The responses of cortical cells to gratings and bars were compared. The excitatory and inhibitory on-and off-zones of a simple cell are composed of on- and off-subfields of CGL. Any zone is formed by an opponent pair of subfields one of which gives an excitatory effect, the other — inhibitory. Such organization assumes the linear properties of a simple field. The deviations from linearity are due to spatial dis-placements of the subfields, heterogeneity of subfields, or the absence of one subfield in the opponent pair. Subfields may be both phasic and tonic, even in the same RF. Analysis of the most common type of a complex cell with modulated responses against unmodulated background shows that a mask eliminating stimulation of any half of the RF causes (according to the theory of filtres) increasing the bandwidth due to the increase or the appearance of responses to side low and high frequencies. The modulated components of the responses from both halves of the RF are out of phase. Analysis of this fact and the responses to thin bars suggests that a complex field is formed by linear and nonlinear subsystems converging onto output neuron. Other types of complex fields are organized by different combinations of subsystems. Limited in area by masking the RF responds to much higher spatial frequencies than the whole RF. The optimal frequency in two-dimensional spatial frequency characteristics of the RF does not change with orientation. Simple RFs and a part of complex RF calculate the amplitude and the phase of the stimulus, the other part of complex RFs (with unmodulated response) calculate only amplitude. Given all this, the RFs are grating filters of spatial frequency.     

Construction of complex receptive fields in cat primary visual cortex.

In primary visual cortex, neurons are classified into simple cells and complex cells based on their response properties. Although the role of these two cell types in vision is still unknown, an attractive hypothesis is that simple cells are necessary to construct complex receptive fields. This hierarchical model puts forward two main predictions. First, simple cells should connect monosynaptically to complex cells. Second, complex cells should become silent when simple cells are inactivated. We have recently provided evidence for the first prediction, and here we do the same for the second. In summary, our results suggest that the receptive fields of most layer 2+3 complex cells are generated by a mechanism that requires simple cell inputs.     

Mechanism of directional sensitivity of receptive fields in the cat visual cortex

Responses of directional-sensitive neurons in area 17 of the cat's cortex were studied to presentation of two flashing bars of light, one located in the center of the field, the other in the inhibitory zone relative to the center. The order of activation of the stimuli and the time interval between them could be varied; presentation of two bars was thus the analog of a moving stimulus. The inhibitory off-zone located at the entrance to the field from the side of the optimal direction of movement was found to have an initial inhibitory phase, followed by a phase of disinhibition, and again by a second inhibitory phase. Presentation of the bars with different time intervals in cases when stimulation of the center of the field coincided in time with one of the inhibitory phases, led to inhibition of the response, but if stimulation coincided with the phase of disinhibition, it led to facilitation. Phases of disinhibition were not found in the inhibitory zone located at the entrance to the field along the course of a nonoptimal direction of movement. The importance of the temporal characteristics of inhibitory zones for the appearance of directional sensitivity of visual courtical neurons is discussed.     

Investigation of functional organization of receptive fields in the cat visual cortex

Receptive fields of neurons in Area 17 of the visual cortex were investigated in cats. Concentrically shaped fields, fields responding selectively to orientation of a strip or edge, and fields which can be regarded as intermediate between the first two types are described. The boundary between zones of summation and of lateral inhibition coincides in some receptive fields with the boundary between central and peripheral zones with opposite forms of response, while in other fields they do not coincide. For some cells there is no peripheral zone or it may disappear with worsening of the state of function. Cells were observed for which an increase in area of the stimulus in the central zone inhibits the response reaction. Analysis of these data suggests that several cells of the geniculate ganglion converge on some cortical neurons, and several cortical cells on others. An effect of adaptive inhibition was found in which constant illumination of an area in the center of the receptive field inhibits the response in another part. It is shown that this effect is unconnected with the action of scattered light. Constant illumination of the peripheral part of the receptive field deinhibits adaptive inhibition. The boundary between the zones of summation and of lateral inhibition coincides with the boundary between the zones of adaptive inhibition and deinhibition.I. V. Pavlov Institute of Physiology, Academy of Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 1, No. 1, pp. 90–100, July–August, 1969.     

Spatiotemporal organization of simple-cell receptive fields in area 18 of cat''''s cortex

Ｍｏｓｔｓｔｕｄｉｅｓｏｎｔｈｅｒｅｃｅｐｔｉｖｅｆｉｅｌｄ(ＲＦ)ｏｒｇａｎｉｚａｔｉｏｎｏｆｖｉｓｕａｌｃｏｒｔｅｘｎｅｕｒｏｎｓｈａｖｅｆｏｃｕｓｅｄｏｎｉｔｓｓｐａｔｉａｌｓｔｒｕｃｔｕｒｅ.Ｓｔｉｍｕｌｉｉｎｔｈｅｎａｔｕｒａｌｖｉｓｕａｌｗｏｒｌｄ,ｈｏｗｅｖｅｒ,ｉｎｃｌｕｄｅｂｏｔｈｓｐａｔｉａｌａｎｄｔｅｍｐｏｒａｌａｓｐｅｃｔｓ.Ｆｏｒａｍｏｒｅｃｏｍｐｌｅｔｅｆｕｎｃｔｉｏｎａｌｄｅｓｃｒｉｐｔｉｏｎｏｆｔｈｅｖｉｓｕａｌｎｅｕｒｏｎｓ,ｉｔｉｓｎｅｃｅｓｓａｒｙｔｏｉｎｖｅｓｔ…     

Theoretical analysis of a TIME-FREQUENCY-PCNN auditory cortex model

A particular pulsed neural model of the auditory cortex, the Time-Frequency Pulse Coupled Neural Network (TF-PCNN), has shown to decompose its stimulus from the cochlea into characteristic pulse-coded time-frequency (TF) stop and pass regions. A derived sum of spectrograms representation with these zero- or one-valued TF weightings has already been applied for the denoising of speech in a previous work. This decomposition is now related to the concept of TF projection filters, which allows to reinterpret the model equations. The functionality imposed by the model equations can so be accessed and justified from a TF signal processing perspective, in addition to its biological motivation from experimentally observed neurophysiological behavior and simulations.     

Spatiotemporal receptive fields: a dynamical model derived from cortical architectonics

We assume that the mammalian neocortex is built up out of some six layers which differ in their morphology and their external connections. Intrinsic connectivity is largely excitatory, leading to a considerable amount of positive feedback. The majority of cortical neurons can be divided into two main classes: the pyramidal cells, which are said to be excitatory, and local cells (most notably the non-spiny stellate cells), which are said to be inhibitory. The form of the dendritic and axonal arborizations of both groups is discussed in detail. This results in a simplified model of the cortex as a stack of six layers with mutual connections determined by the principles of fibre anatomy. This stack can be treated as a multi-input-multi-output system by means of the linear systems theory of homogeneous layers. The detailed equations for the simulation are derived in the Appendix. The results of the simulations show that the temporal and spatial behaviour of an excitation distribution cannot be treated separately. Further, they indicate specific processing in the different layers and some independence from details of wiring. Finally, the simulation results are applied to the theory of visual receptive fields. This yields some insight into the mechanisms possibly underlying hypercomplexity, putative nonlinearities, lateral inhibition, oscillating cell responses, and velocity-dependent tuning curves.     

The function of the medial superior olive in small mammals: temporal receptive fields in auditory analysis

Traditionally, the medial superior olive, a mammalian auditory brainstem structure, is considered to encode interaural time differences, the main cue for localizing low-frequency sounds. Detection of binaural excitatory and inhibitory inputs are considered as an underlying mechanism. Most small mammals, however, hear high frequencies well beyond 50 kHz and have small interaural distances. Therefore, they can not use interaural time differences for sound localization and yet possess a medial superior olive. Physiological studies in bats revealed that medial superior olive cells show similar interaural time difference coding as in larger mammals tuned to low-frequency hearing. Their interaural time difference sensitivity, however, is far too coarse to serve in sound localization. Thus, interaural time difference sensitivity in medial superior olive of small mammals is an epiphenomenon. We propose that the original function of the medial superior olive is a binaural cooperation causing facilitation due to binaural excitation. Lagging inhibitory inputs, however, suppress reverberations and echoes from the acoustic background. Thereby, generation of antagonistically organized temporal fields is the basic and original function of the mammalian medial superior olive. Only later in evolution with the advent of larger mammals did interaural distances, and hence interaural time differences, became large enough to be used as cues for sound localization of low-frequency stimuli. Accepted: 28 February 2000