An olfactory recognition model based on spatio-temporal encoding of odor quality in the olfactory bulb

In order to study the problem how the olfactory neural system processes the odorant molecular information for constructing the olfactory image of each object, we present a dynamic model of the olfactory bulb constructed on the basis of well-established experimental and theoretical results. The information relevant to a single odor, i.e. its constituent odorant molecules and their mixing ratios, are encoded into a spatio-temporal pattern of neural activity in the olfactory bulb, where the activity pattern corresponds to a limit cycle attractor in the mitral cell network. The spatio-temporal pattern consists of a temporal sequence of spatial firing patterns: each constituent molecule is encoded into a single spatial pattern, and the order of magnitude of the mixing ratio is encoded into the temporal sequence. The formation of a limit cycle attractor under the application of a novel odor is carried out based on the intensity-to-time-delay encoding scheme. The dynamic state of the olfactory bulb, which has learned many odors, becomes a randomly itinerant state in which the current firing state of the bulb itinerates randomly among limit cycle attractors corresponding to the learned odors. The recognition of an odor is generated by the dynamic transition in the network from the randomly itinerant state to a limit cycle attractor state relevant to the odor, where the transition is induced by the short-term synaptic changes made according to the Hebbian rule under the application of the odor stimulus. Received: 28 July 1997 / Accepted in revised form: 6 May 1998     

Processing of Auditory Midbrain Interspike Intervals by Model Neurons

A question central to sensory processing is how signal information is encoded and processed by single neurons. Stimulus features can be represented through rate coding (via firing rate), temporal coding (via firing synchronization to temporal periodicities), or temporal encoding (via intricate patterns of spike trains). Of the three, examples of temporal encoding are the least documented. One region in which temporal encoding is currently being explored is the auditory midbrain. Midbrain neurons in the plainfin midshipman generate different interspike interval (ISI) distributions depending on the frequencies of the concurrent vocal signals. However, these distributions differ only along certain lengths of ISIs, so that any neurons trying to distinguish the distributions would have to respond selectively to specific ISI ranges. We used this empirical observation as a realistic challenge with which to explore the plausibility of ISI-tuned neurons that could validate this form of temporal encoding. The resulting modeled cells—point neurons optimized through multidimensional searching—were successfully tuned to discriminate patterns in specific ranges of ISIs. Achieving this task, particularly with simplified neurons, strengthens the credibility of ISI coding in the brain and lends credence to its role in auditory processing.     

Impaired Temporal Processing of Tactile and Proprioceptive Stimuli in Cerebellar Degeneration

Performance of timed motor sequences relies on the cerebellum and basal ganglia, which integrate proprioceptive information during the motor task and set internal timing mechanisms. Accordingly, these structures are also involved in other temporal processes, such as the discrimination of the different afferent information in the domain of time. In the present study we tested temporal processing of proprioceptive and tactile stimuli in 20 patients with neurodegenerative cerebellar ataxia and 20 age- and sex-matched healthy subjects. Tactile temporal discrimination threshold was defined as the value at which subjects recognized the two stimuli as asynchronous. Temporal discrimination movement threshold of the first dorsal interosseous and flexor carpi radialis was defined as the shortest interval between two paired electrical stimuli in which the subjects blindfolded perceived two separate index finger abductions and wrist flexions. Both tactile and movement temporal discrimination thresholds were higher in patients with cerebellar ataxia. No correlation was found with disease duration and severity. Our study demonstrates that temporal processing of tactile and proprioceptive stimuli is impaired in patients with cerebellar neurodegeneration and highlights the involvement of cerebellum in temporal processing of somatosensory stimuli of different type.     

Identifying temporal codes in spontaneously active sensory neurons

The manner in which information is encoded in neural signals is a major issue in Neuroscience. A common distinction is between rate codes, where information in neural responses is encoded as the number of spikes within a specified time frame (encoding window), and temporal codes, where the position of spikes within the encoding window carries some or all of the information about the stimulus. One test for the existence of a temporal code in neural responses is to add artificial time jitter to each spike in the response, and then assess whether or not information in the response has been degraded. If so, temporal encoding might be inferred, on the assumption that the jitter is small enough to alter the position, but not the number, of spikes within the encoding window. Here, the effects of artificial jitter on various spike train and information metrics were derived analytically, and this theory was validated using data from afferent neurons of the turtle vestibular and paddlefish electrosensory systems, and from model neurons. We demonstrate that the jitter procedure will degrade information content even when coding is known to be entirely by rate. For this and additional reasons, we conclude that the jitter procedure by itself is not sufficient to establish the presence of a temporal code.     

See me, hear me, touch me: multisensory integration in lateral occipital-temporal cortex

Our understanding of multisensory integration has advanced because of recent functional neuroimaging studies of three areas in human lateral occipito-temporal cortex: superior temporal sulcus, area LO and area MT (V5). Superior temporal sulcus is activated strongly in response to meaningful auditory and visual stimuli, but responses to tactile stimuli have not been well studied. Area LO shows strong activation in response to both visual and tactile shape information, but not to auditory representations of objects. Area MT, an important region for processing visual motion, also shows weak activation in response to tactile motion, and a signal that drops below resting baseline in response to auditory motion. Within superior temporal sulcus, a patchy organization of regions is activated in response to auditory, visual and multisensory stimuli. This organization appears similar to that observed in polysensory areas in macaque superior temporal sulcus, suggesting that it is an anatomical substrate for multisensory integration. A patchy organization might also be a neural mechanism for integrating disparate representations within individual sensory modalities, such as representations of visual form and visual motion.     

Temporal encoding in nervous systems: A rigorous definition

We propose a rigorous definition for the termtemporal encoding as it is applied to schemes for the representation of information withinpatterns of neuronal action potentials, and distinguish temporal encoding schemes from those based on window-averagedmean rate encoding. The definition relies on the identification of anencoding time window, defined as the duration of a neuron's spike train assumed to correspond to a single symbol in the neural code. The duration of the encoding time window is dictated by the time scale of the information being encoded. We distinguish between the concepts of theencoding time window and theintegration time window, the latter of which is defined as the duration of a stimulus signal that affects the response of the neuron. We note that the duration of the encoding and integration windows might be significantly different. We also present objective, experimentally assessable criteria for identifying neurons and neuronal ensembles that utilize temporal encoding to any significant extent. The definitions and criteria are made rigorous within the contexts of several commonly used analytical approaches, including thestimulus reconstruction analysis technique. Several examples are presented to illustrate the distinctions between and relative capabilities of rate encoding and temporal encoding schemes. We also distinguish our usage oftemporal encoding from the termtemporal coding, which is commonly used in reference to the representation of information about thetiming of events by rate encoding schemes.     

Neural encoding schemes of tactile information in afferent activity of the vibrissal system

When rats acquire sensory information by actively moving their vibrissae, a neural code is manifested at different levels of the sensory system. Behavioral studies in tactile discrimination agree that rats can distinguish different roughness surfaces by whisking their vibrissae. The present study explores the existence of neural encoding in the afferent activity of one vibrissal nerve. Two neural encoding schemes based on “events” were proposed (cumulative event count and median inter-event time). The events were detected by using an event detection algorithm based on multiscale decomposition of the signal (Continuous Wavelet Transform). The encoding schemes were quantitatively evaluated through the maximum amount of information which was obtained by the Shannon’s mutual information formula. Moreover, the effect of difference distances between rat snout and swept surfaces on the information values was also studied. We found that roughness information was encoded by events of 0.8 ms duration in the cumulative event count and event of 1.0 to 1.6 ms duration in the median inter-event count. It was also observed that an extreme decrease of the distance between rat snout and swept surfaces significantly reduces the information values and the capacity to discriminate among the sweep situations.     

Tactile and Proprioceptive Temporal Discrimination Are Impaired in Functional Tremor

Background and Methods

In order to obtain further information on the pathophysiology of functional tremor, we assessed tactile discrimination threshold and proprioceptive temporal discrimination motor threshold values in 11 patients with functional tremor, 11 age- and sex-matched patients with essential tremor and 13 healthy controls.

Results

Tactile discrimination threshold in both the right and left side was significantly higher in patients with functional tremor than in the other groups. Proprioceptive temporal discrimination threshold for both right and left side was significantly higher in patients with functional and essential tremor than in healthy controls. No significant correlation between discrimination thresholds and duration or severity of tremor was found.

Conclusions

Temporal processing of tactile and proprioceptive stimuli is impaired in patients with functional tremor. The mechanisms underlying this impaired somatosensory processing and possible ways to apply these findings clinically merit further research.     

Speech-evoked activity in primary auditory cortex: effects of voice onset time

Neural encoding of temporal speech features is a key component of acoustic and phonetic analyses. We examined the temporal encoding of the syllables /da/ and /ta/, which differ along the temporally based, phonetic parameter of voice onset time (VOT), in primary auditory cortex (A1) of awake monkeys using concurrent multilaminar recordings of auditory evoked potentials (AEP), the derived current source density, and multiunit activity. A general sequence of A1 activation consisting of a lamina-specific profile of parallel and sequential excitatory and inhibitory processes is described. VOT is encoded in the temporal response patterns of phase-locked activity to the periodic speech segments and by “on” responses to stimulus and voicing onset. A transformation occurs between responses in the thalamocortical (TC) fiber input and A1 cells. TC fibers are more likely to encode VOT with “on” responses to stimulus onset followed by phase-locked responses during the voiced segment, whereas A1 responses are more likely to exhibit transient responses both to stimulus and voicing onset. Relevance to subcortical speech processing, the human AEP and speech psychoacoustics are discussed. A mechanism for categorical differentiation of voiced and unvoiced consonants is proposed.     

Tactile motion and pattern processing assessed with high-field FMRI

Processing of motion and pattern has been extensively studied in the visual domain, but much less in the somatosensory system. Here, we used ultra-high-field functional magnetic resonance imaging (fMRI) at 7 Tesla to investigate the neuronal correlates of tactile motion and pattern processing in humans under tightly controlled stimulation conditions. Different types of dynamic stimuli created the sensation of moving or stationary bar patterns during passive touch. Activity in somatosensory cortex was increased during both motion and pattern processing and modulated by motion directionality in primary and secondary somatosensory cortices (SI and SII) as well as by pattern orientation in the anterior intraparietal sulcus. Furthermore, tactile motion and pattern processing induced activity in the middle temporal cortex (hMT+/V5) and in the inferior parietal cortex (IPC), involving parts of the supramarginal und angular gyri. These responses covaried with subjects' individual perceptual performance, suggesting that hMT+/V5 and IPC contribute to conscious perception of specific tactile stimulus features. In addition, an analysis of effective connectivity using psychophysiological interactions (PPI) revealed increased functional coupling between SI and hMT+/V5 during motion processing, as well as between SI and IPC during pattern processing. This connectivity pattern provides evidence for the direct engagement of these specialized cortical areas in tactile processing during somesthesis.     

Differential but complementary mnemonic functions of the hippocampus and subiculum

In this study we describe how the hippocampus and subiculum act in concert to encode information in a spatial delayed-nonmatch-to-sample (DNMS) task. This encoding was functionally partitioned between neurons within subiculum and hippocampus to uniquely identify trial-specific information accounting for both spatial and temporal constraints on performance within and between trials. Encoding by subicular neurons in the task was normally accurate and specific, but only if delays were shorter than 15 s, whereas trial-specific information encoded by hippocampal neurons was subject to strong biases from prior trial sequences and was accessible only when delays exceeded 15 s. The two structures operated in a complementary manner to encode information correctly on 75% of all trials using the above strategies. The remaining 25% of trials were at risk due to inherent idiosyncrasies by which hippocampal and subicular neurons encoded information and became errors when the random sequence of trials conflicted with these constraints.     

Audio-Tactile Integration and the Influence of Musical Training

Perception of our environment is a multisensory experience; information from different sensory systems like the auditory, visual and tactile is constantly integrated. Complex tasks that require high temporal and spatial precision of multisensory integration put strong demands on the underlying networks but it is largely unknown how task experience shapes multisensory processing. Long-term musical training is an excellent model for brain plasticity because it shapes the human brain at functional and structural levels, affecting a network of brain areas. In the present study we used magnetoencephalography (MEG) to investigate how audio-tactile perception is integrated in the human brain and if musicians show enhancement of the corresponding activation compared to non-musicians. Using a paradigm that allowed the investigation of combined and separate auditory and tactile processing, we found a multisensory incongruency response, generated in frontal, cingulate and cerebellar regions, an auditory mismatch response generated mainly in the auditory cortex and a tactile mismatch response generated in frontal and cerebellar regions. The influence of musical training was seen in the audio-tactile as well as in the auditory condition, indicating enhanced higher-order processing in musicians, while the sources of the tactile MMN were not influenced by long-term musical training. Consistent with the predictive coding model, more basic, bottom-up sensory processing was relatively stable and less affected by expertise, whereas areas for top-down models of multisensory expectancies were modulated by training.     

Enhanced intersubject correlations during movie viewing correlate with successful episodic encoding

While much has been learned regarding the neural substrates supporting episodic encoding using highly controlled experimental protocols, relatively little is known regarding the neural bases of episodic encoding of real-world events. In an effort to examine this issue, we measured fMRI activity while observers viewed a novel TV sitcom. Three weeks later, subsequent memory (SM) for the narrative content of movie events was assessed. We analyzed the encoding data for intersubject correlations (ISC) based on subjects' subsequent memory (ISC-SM) performance to identify brain regions whose BOLD response is significantly more correlated across subjects during portions of the movie that are successfully as compared to unsuccessfully encoded. These regions include the parahippocampal gyrus, superior temporal gyrus, anterior temporal poles, and the temporal-parietal junction. Further analyses reveal (1) that these correlated regions can display distinct activation profiles and (2) that the results seen with the ISC-SM analysis are complementary to more traditional linear models and allow analysis of complex time course data. Thus, the ISC-SM analysis extends traditional subsequent memory findings to a rich, dynamic and more ecologically valid situation.     

Coding efficiency and information rates in transmembrane signaling

A variety of cell types responds to hormonal stimuli by repetitive spikes in the intracellular concentration of calcium ([Ca(2+)](i)) which have been demonstrated to encode information in their frequency, amplitude, and duration. These [Ca(2+)](i)-spike trains are able to specifically regulate distinct cellular functions. Using a mathematical model for receptor-controlled [Ca(2+)](i) oscillations in hepatocytes we investigate the encoding of fluctuating hormonal signals in [Ca(2+)](i)-spike trains. The transmembrane information transfer is quantified by using an information-theoretic reverse-engineering approach which allows to reconstruct the dynamic hormonal stimulus from the [Ca(2+)](i)-spike trains. This approach allows to estimate the accuracy of coding as well as the rate of transmembrane information transfer. We found that up to 87% of the dynamic stimulus information can be encoded in the [Ca(2+)](i)-spike train at a maximum information transfer rate of 1.1 bit per [Ca(2+)](i)-spike. These numerical results for humoral information transfer are in the same order as in a number of sensory neuronal systems despite several orders of magnitude different time scales of operation suggesting a universal principle of information processing in both biological systems.     

Neural mechanism of dynamic responses of neurons in inferior temporal cortex in face perception

Understanding the neural mechanisms of object and face recognition is one of the fundamental challenges of visual neuroscience. The neurons in inferior temporal (IT) cortex have been reported to exhibit dynamic responses to face stimuli. However, little is known about how the dynamic properties of IT neurons emerge in the face information processing. To address this issue, we made a model of IT cortex, which performs face perception via an interaction between different IT networks. The model was based on the face information processed by three resolution maps in early visual areas. The network model of IT cortex consists of four kinds of networks, in which the information about a whole face is combined with the information about its face parts and their arrangements. We show here that the learning of face stimuli makes the functional connections between these IT networks, causing a high spike correlation of IT neuron pairs. A dynamic property of subthreshold membrane potential of IT neuron, produced by Hodgkin–Huxley model, enables the coordination of temporal information without changing the firing rate, providing the basis of the mechanism underlying face perception. We show also that the hierarchical processing of face information allows IT cortex to perform a “coarse-to-fine” processing of face information. The results presented here seem to be compatible with experimental data about dynamic properties of IT neurons.     

Adaptive Spike Threshold Enables Robust and Temporally Precise Neuronal Encoding

Neural processing rests on the intracellular transformation of information as synaptic inputs are translated into action potentials. This transformation is governed by the spike threshold, which depends on the history of the membrane potential on many temporal scales. While the adaptation of the threshold after spiking activity has been addressed before both theoretically and experimentally, it has only recently been demonstrated that the subthreshold membrane state also influences the effective spike threshold. The consequences for neural computation are not well understood yet. We address this question here using neural simulations and whole cell intracellular recordings in combination with information theoretic analysis. We show that an adaptive spike threshold leads to better stimulus discrimination for tight input correlations than would be achieved otherwise, independent from whether the stimulus is encoded in the rate or pattern of action potentials. The time scales of input selectivity are jointly governed by membrane and threshold dynamics. Encoding information using adaptive thresholds further ensures robust information transmission across cortical states i.e. decoding from different states is less state dependent in the adaptive threshold case, if the decoding is performed in reference to the timing of the population response. Results from in vitro neural recordings were consistent with simulations from adaptive threshold neurons. In summary, the adaptive spike threshold reduces information loss during intracellular information transfer, improves stimulus discriminability and ensures robust decoding across membrane states in a regime of highly correlated inputs, similar to those seen in sensory nuclei during the encoding of sensory information.     

Coding processes involved in the cortical representation of complex tactile stimuli

To understand how information is coded in the primary somatosensory cortex (S1) we need to decipher the relationship between neural activity and tactile stimuli. Such a relationship can be formally measured by mutual information. The present study was designed to determine how S1 neuronal populations code for the multidimensional kinetic features (i.e. random, time-varying patterns of force) of complex tactile stimuli, applied at different locations of the rat forepaw. More precisely, the stimulus localization and feature extraction were analyzed as two independent processes, using both rate coding and temporal coding strategies. To model the process of stimulus kinetic feature extraction, multidimensional stimuli were projected onto lower dimensional subspace and then clustered according to their similarity. Different combinations of stimuli clustering were applied to differentiate each stimulus identification process. Information analyses show that both processes are synergistic, this synergy is enhanced within the temporal coding framework. The stimulus localization process is faster than the stimulus feature extraction process. The latter provides more information quantity with rate coding strategy, whereas the localization process maximizes the mutual information within the temporal coding framework. Therefore, combining mutual information analysis with robust clustering of complex stimuli provides a framework to study neural coding mechanisms related to complex stimuli discrimination.     

Encoding of Temporal Information by Timing,Rate, and Place in Cat Auditory Cortex

A central goal in auditory neuroscience is to understand the neural coding of species-specific communication and human speech sounds. Low-rate repetitive sounds are elemental features of communication sounds, and core auditory cortical regions have been implicated in processing these information-bearing elements. Repetitive sounds could be encoded by at least three neural response properties: 1) the event-locked spike-timing precision, 2) the mean firing rate, and 3) the interspike interval (ISI). To determine how well these response aspects capture information about the repetition rate stimulus, we measured local group responses of cortical neurons in cat anterior auditory field (AAF) to click trains and calculated their mutual information based on these different codes. ISIs of the multiunit responses carried substantially higher information about low repetition rates than either spike-timing precision or firing rate. Combining firing rate and ISI codes was synergistic and captured modestly more repetition information. Spatial distribution analyses showed distinct local clustering properties for each encoding scheme for repetition information indicative of a place code. Diversity in local processing emphasis and distribution of different repetition rate codes across AAF may give rise to concurrent feed-forward processing streams that contribute differently to higher-order sound analysis.     

Dose-to-duration encoding and signaling beyond saturation in intracellular signaling networks

The cellular response elicited by an environmental cue typically varies with the strength of the stimulus. For example, in the yeast Saccharomyces cerevisiae, the concentration of mating pheromone determines whether cells undergo vegetative growth, chemotropic growth, or mating. This implies that the signaling pathways responsible for detecting the stimulus and initiating a response must transmit quantitative information about the intensity of the signal. Our previous experimental results suggest that yeast encode pheromone concentration as the duration of the transmitted signal. Here we use mathematical modeling to analyze possible biochemical mechanisms for performing this “dose-to-duration” conversion. We demonstrate that modulation of signal duration increases the range of stimulus concentrations for which dose-dependent responses are possible; this increased dynamic range produces the counterintuitive result of “signaling beyond saturation” in which dose-dependent responses are still possible after apparent saturation of the receptors. We propose a mechanism for dose-to-duration encoding in the yeast pheromone pathway that is consistent with current experimental observations. Most previous investigations of information processing by signaling pathways have focused on amplitude encoding without considering temporal aspects of signal transduction. Here we demonstrate that dose-to-duration encoding provides cells with an alternative mechanism for processing and transmitting quantitative information about their surrounding environment. The ability of signaling pathways to convert stimulus strength into signal duration results directly from the nonlinear nature of these systems and emphasizes the importance of considering the dynamic properties of signaling pathways when characterizing their behavior. Understanding how signaling pathways encode and transmit quantitative information about the external environment will not only deepen our understanding of these systems but also provide insight into how to reestablish proper function of pathways that have become dysregulated by disease.