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Functional analysis of ultra high information rates conveyed by rat vibrissal primary afferents.

ABSTRACT: Sensory receptors determine the type and the quantity of information available for perception. Here, we quantified and characterized the information transferred by primary afferents in the rat whisker system using neural system identification. Quantification of "how much" information is conveyed by primary afferents, using the direct method (DM), a classical information theoretic tool, revealed that primary afferents transfer huge amounts of information (up to 529 bits/s). Information theoretic analysis of instantaneous spike-triggered kinematic stimulus features was used to gain functional insight on "what" is coded by primary afferents. Amongst the kinematic variables tested--position, velocity, and acceleration--primary afferent spikes encoded velocity best. The other two variables contributed to information transfer, but only if combined with velocity. We further revealed three additional characteristics that play a role in information transfer by primary afferents. Firstly, primary afferent spikes show preference for well separated multiple stimuli (i.e., well separated sets of combinations of the three instantaneous kinematic variables). Secondly, neurons are sensitive to short strips of the stimulus trajectory (up to 10 ms pre-spike time), and thirdly, they show spike patterns (precise doublet and triplet spiking). In order to deal with these complexities, we used a flexible probabilistic neuron model fitting mixtures of Gaussians to the spike triggered stimulus distributions, which quantitatively captured the contribution of the mentioned features and allowed us to achieve a full functional analysis of the total information rate indicated by the DM. We found that instantaneous position, velocity, and acceleration explained about 50% of the total information rate. Adding a 10 ms pre-spike interval of stimulus trajectory achieved 80-90%. The final 10-20% were found to be due to non-linear coding by spike bursts.

SUBMITTER: Chagas AM

PROVIDER: S-EPMC3852094 | biostudies-literature | 2013

REPOSITORIES: biostudies-literature

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Project description:The rat vibrissal system is an important model for the study of somatosensation, but the small size and rapid speed of the vibrissae have precluded measuring precise vibrissal-object contact sequences during behavior. We used a laser light sheet to quantify, with 1 ms resolution, the spatiotemporal structure of whisker-surface contact as five naïve rats freely explored a flat, vertical glass wall. Consistent with previous work, we show that the whisk cycle cannot be uniquely defined because different whiskers often move asynchronously, but that quasi-periodic (~8 Hz) variations in head velocity represent a distinct temporal feature on which to lock analysis. Around times of minimum head velocity, whiskers protract to make contact with the surface, and then sustain contact with the surface for extended durations (~25-60 ms) before detaching. This behavior results in discrete temporal windows in which large numbers of whiskers are in contact with the surface. These "sustained collective contact intervals" (SCCIs) were observed on 100% of whisks for all five rats. The overall spatiotemporal structure of the SCCIs can be qualitatively predicted based on information about head pose and the average whisk cycle. In contrast, precise sequences of whisker-surface contact depend on detailed head and whisker kinematics. Sequences of vibrissal contact were highly variable, equally likely to propagate in all directions across the array. Somewhat more structure was found when sequences of contacts were examined on a row-wise basis. In striking contrast to the high variability associated with contact sequences, a consistent feature of each SCCI was that the contact locations of the whiskers on the glass converged and moved more slowly on the sheet. Together, these findings lead us to propose that the rat uses a strategy of "windowed sampling" to extract an object's spatial features: specifically, the rat spatially integrates quasi-static mechanical signals across whiskers during the period of sustained contact, resembling an "enclosing" haptic procedure.

Project description:Humans not only process and compare magnitude information such as size, duration, and number perceptually, but they also communicate about these properties using language. In this respect, a relevant class of lexical items are so-called scalar adjectives like "big," "long," "loud," and so on which refer to magnitude information. It has been proposed that humans use an amodal and abstract representation format shared by different dimensions, called the generalised magnitude system (GMS). In this paper, we test the hypothesis that scalar adjectives are symbolic references to GMS representations, and, therefore, GMS gets involved in processing their meaning. Previously, a parallel hypothesis on the relation between number symbols and GMS representations has been tested with the size congruity paradigm. The results of these experiments showed interference between the processing of number symbols and the processing of physical (font-) size. In the first three experiments of the present study (total N = 150), we used the size congruity paradigm and the same/different task to look at the potential interaction between physical size magnitude and numerical magnitude expressed by number words. In the subsequent three experiments (total N = 149), we looked at a parallel potential interaction between physical size magnitude and scalar adjective meaning. In the size congruity paradigm, we observed interference between the processing of the numerical value of number words and the meaning of scalar adjectives, on the one hand, and physical (font-) size, on the other hand, when participants had to judge the number words or the adjectives (while ignoring physical size). No interference was obtained for the reverse situation, i.e., when participants judged the physical font size (while ignoring numerical value or meaning). The results of the same/different task for both number words and scalar adjectives strongly suggested that the interference that was observed in the size congruity paradigm was likely due to a response conflict at the decision stage of processing rather than due to the recruitment of GMS representations. Taken together, it can be concluded that the size congruity paradigm does not provide evidence in support the hypothesis that GMS representations are used in the processing of number words or scalar adjectives. Nonetheless, the hypothesis we put forward about scalar adjectives is still is a promising potential line of research. We make a number of suggestions for how this hypothesis can be explored in future studies.

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Functional analysis of ultra high information rates conveyed by rat vibrissal primary afferents.

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