Temporal processing and adaptation in the songbird auditory forebrain

Songbird auditory neurons must encode the dynamics of natural sounds at many volumes. We investigated how neural coding depends on the distribution of stimulus intensities. Using reverse-correlation, we modeled responses to amplitude-modulated sounds as the output of a linear filter and a nonlinear gain function, then asked how filters and nonlinearities depend on the stimulus mean and variance. Filter shape depended strongly on mean amplitude (volume): at low mean, most neurons integrated sound over many milliseconds, while at high mean, neurons responded more to local changes in amplitude. Increasing the variance (contrast) of amplitude modulations had less effect on filter shape but decreased the gain of firing in most cells. Both filter and gain changes occurred rapidly after a change in statistics, suggesting that they represent nonlinearities in processing. These changes may permit neurons to signal effectively over a wider dynamic range and are reminiscent of findings in other sensory systems.     

Category-Specific Processing of Scale-Invariant Sounds in Infancy

Increasing evidence suggests that the natural world has a special status for our sensory and cognitive functioning. The mammalian sensory system is hypothesized to have evolved to encode natural signals in an efficient manner. Exposure to natural stimuli, but not to artificial ones, improves learning and cognitive function. Scale-invariance, the property of exhibiting the same statistical structure at different spatial or temporal scales, is common to naturally occurring sounds. We recently developed a 3-parameter model to capture the essential characteristics of water sounds, and from this generated both scale-invariant and variable-scale sounds. In a previous study, we found that adults perceived a wide range of the artificial scale-invariant, but not the variable-scale, sounds as instances of natural sounds. Here, we explored the ontogenetic origins of these effects by investigating how young infants perceive and categorize scale-invariant acoustic stimuli. Even though they have several months of experience with natural water sounds, infants aged 5 months did not show a preference, in the first experiment, for the instances of the scale-invariant sounds rated as typical water-like sounds by adults over non-prototypical, but still scale-invariant instances. Scale-invariance might thus be a more relevant factor for the perception of natural signals than simple familiarity. In a second experiment, we thus directly compared infants'' perception of scale-invariant and variable-scale sounds. When habituated to scale-invariant sounds, infants looked significantly longer to a change in sound category from scale-invariant to variable-scale sounds, whereas infants habituated to variable-scale sounds showed no such difference. These results suggest that infants were able to form a perceptual category of the scale-invariant, but not variable-scale sounds. These findings advance the efficient coding hypothesis, and suggest that the advantage for perceiving and learning about the natural world is evident from the first months of life.     

How Does the Extraction of Local and Global Auditory Regularities Vary with Context?

How does the human brain extract regularities from its environment? There is evidence that short range or ‘local’ regularities (within seconds) are automatically detected by the brain while long range or ‘global’ regularities (over tens of seconds or more) require conscious awareness. In the present experiment, we asked whether participants'' attention was needed to acquire such auditory regularities, to detect their violation or both. We designed a paradigm in which participants listened to predictable sounds. Subjects could be distracted by a visual task at two moments: when they were first exposed to a regularity or when they detected violations of this regularity. MEG recordings revealed that early brain responses (100–130 ms) to violations of short range regularities were unaffected by visual distraction and driven essentially by local transitional probabilities. Based on global workspace theory and prior results, we expected that visual distraction would eliminate the long range global effect, but unexpectedly, we found the contrary, i.e. late brain responses (300–600 ms) to violations of long range regularities on audio-visual trials but not on auditory only trials. Further analyses showed that, in fact, visual distraction was incomplete and that auditory and visual stimuli interfered in both directions. Our results show that conscious, attentive subjects can learn the long range dependencies present in auditory stimuli even while performing a visual task on synchronous visual stimuli. Furthermore, they acquire a complex regularity and end up making different predictions for the very same stimulus depending on the context (i.e. absence or presence of visual stimuli). These results suggest that while short-range regularity detection is driven by local transitional probabilities between stimuli, the human brain detects and stores long-range regularities in a highly flexible, context dependent manner.     

The Human Brain Maintains Contradictory and Redundant Auditory Sensory Predictions

Computational and experimental research has revealed that auditory sensory predictions are derived from regularities of the current environment by using internal generative models. However, so far, what has not been addressed is how the auditory system handles situations giving rise to redundant or even contradictory predictions derived from different sources of information. To this end, we measured error signals in the event-related brain potentials (ERPs) in response to violations of auditory predictions. Sounds could be predicted on the basis of overall probability, i.e., one sound was presented frequently and another sound rarely. Furthermore, each sound was predicted by an informative visual cue. Participants’ task was to use the cue and to discriminate the two sounds as fast as possible. Violations of the probability based prediction (i.e., a rare sound) as well as violations of the visual-auditory prediction (i.e., an incongruent sound) elicited error signals in the ERPs (Mismatch Negativity [MMN] and Incongruency Response [IR]). Particular error signals were observed even in case the overall probability and the visual symbol predicted different sounds. That is, the auditory system concurrently maintains and tests contradictory predictions. Moreover, if the same sound was predicted, we observed an additive error signal (scalp potential and primary current density) equaling the sum of the specific error signals. Thus, the auditory system maintains and tolerates functionally independently represented redundant and contradictory predictions. We argue that the auditory system exploits all currently active regularities in order to optimally prepare for future events.     

Human cerebrocortical potentials evoked by stimulation of the dorsal nerve of the penis

Cortical evoked potentials resulting from stimulation of the dorsal nerve of the penis (DNP) provide a unique opportunity to document the cortical localization of sexual sensory representation in man. The DNP supplies sensory axons to the major portion of the human phallus, including the penile shaft and glans. Animal and human studies indicate that this nerve plays a crucial role in erection and ejaculation. Direct cortical evoked responses to DNP electrical stimulation were recorded in patients undergoing preoperative evaluation for resection of epileptic foci. These studies provided evidence that the primary sensory cortex contains a large area of cortex devoted to the afferent fibers of the DNP and that the sensory field is in a different location than previously described. The location and distribution of this response indicated the need for revision of the traditional concept of the sensory cortical homunculus.     

Optimal Prediction of Moving Sound Source Direction in the Owl

Capturing nature’s statistical structure in behavioral responses is at the core of the ability to function adaptively in the environment. Bayesian statistical inference describes how sensory and prior information can be combined optimally to guide behavior. An outstanding open question of how neural coding supports Bayesian inference includes how sensory cues are optimally integrated over time. Here we address what neural response properties allow a neural system to perform Bayesian prediction, i.e., predicting where a source will be in the near future given sensory information and prior assumptions. The work here shows that the population vector decoder will perform Bayesian prediction when the receptive fields of the neurons encode the target dynamics with shifting receptive fields. We test the model using the system that underlies sound localization in barn owls. Neurons in the owl’s midbrain show shifting receptive fields for moving sources that are consistent with the predictions of the model. We predict that neural populations can be specialized to represent the statistics of dynamic stimuli to allow for a vector read-out of Bayes-optimal predictions.     

Independence of echo-threshold and echo-delay in the barn owl

Despite their prevalence in nature, echoes are not perceived as events separate from the sounds arriving directly from an active source, until the echo's delay is long. We measured the head-saccades of barn owls and the responses of neurons in their auditory space-maps while presenting a long duration noise-burst and a simulated echo. Under this paradigm, there were two possible stimulus segments that could potentially signal the location of the echo. One was at the onset of the echo; the other, after the offset of the direct (leading) sound, when only the echo was present. By lengthening the echo's duration, independently of its delay, spikes and saccades were evoked by the source of the echo even at delays that normally evoked saccades to only the direct source. An echo's location thus appears to be signaled by the neural response evoked after the offset of the direct sound.     

Neural representation of the acoustic biotope

Cats were stimulated with tones and with natural sounds selected from the normal acoustic environment of the animal. Neural activity evoked by the natural sounds and tones was recorded in the cochlear nucleus and in the medial geniculate body. The set of biological sounds proved to be effective in influencing neural activity of single cells at both levels in the auditory system. At the level of the cochlear nucleus the response of a neuron evoked by a natural sound stimulus could be understood reasonably well on the basis of the structure of the spectrograms of the natural sounds and the unit's responses to tones. At the level of the medial geniculate body analysis with tones did not provide sufficient information to explain the responses to natural sounds. At this level the use of an ensemble of natural sound stimuli allows the investigation of neural properties, which are not seen by analysis with simple artificial stimuli. Guidelines for the construction of an ensemble of complex natural sound stimuli, based on the ecology and ethology of the animal under investigation are discussed. This stimulus ensemble is defined as the Acoustic Biotope.     

Adaptation accentuates responses of fly motion-sensitive visual neurons to sudden stimulus changes

Adaptation in sensory and neuronal systems usually leads to reduced responses to persistent or frequently presented stimuli. In contrast to simple fatigue, adapted neurons often retain their ability to encode changes in stimulus intensity and to respond when novel stimuli appear. We investigated how the level of adaptation of a fly visual motion-sensitive neuron affects its responses to discontinuities in the stimulus, i.e. sudden brief changes in one of the stimulus parameters (velocity, contrast, grating orientation and spatial frequency). Although the neuron''s overall response decreased gradually during ongoing motion stimulation, the response transients elicited by stimulus discontinuities were preserved or even enhanced with adaptation. Moreover, the enhanced sensitivity to velocity changes by adaptation was not restricted to a certain velocity range, but was present regardless of whether the neuron was adapted to a baseline velocity below or above its steady-state velocity optimum. Our results suggest that motion adaptation helps motion-sensitive neurons to preserve their sensitivity to novel stimuli even in the presence of strong tonic stimulation, for example during self-motion.     

Temporal integration in auditory sensory memory: neuromagnetic evidence

The cortical mechanisms of auditory sensory memory were investigated by analysis of neuromagnetic evoked responses. The major deflection of the auditory evoked field (N100m) appears to comprise an early posterior component (N100m^P) and a late anterior component (N100m^A) which is sensitive to temporal factors. When pairs of identical sounds are presented at intervals less than about 250 msec, the second sound evokes N100m^A with enhanced amplitude at a latency of about 150 msec. We suggest that N100m^A may index the activity of two distinct processes in auditory sensory memory. Its recovery cycle may reflect the activity of a memory trace which, according to previous studies, can retain processed information about an auditory sequence for about 10 sec. The enhancement effect may reflect the activity of a temporal integration process, whose time constant is such that sensation persists for 200–300 msec after stimulus offset, and so serves as a short memory store. Sound sequences falling within this window of integration seem to be coded holistically as unitary events.     

Quantitative Assessment of Cortical Auditory-tactile Processing in Children with Disabilities

Objective and easy measurement of sensory processing is extremely difficult in nonverbal or vulnerable pediatric patients. We developed a new methodology to quantitatively assess children''s cortical processing of light touch, speech sounds and the multisensory processing of the 2 stimuli, without requiring active subject participation or causing children discomfort. To accomplish this we developed a dual channel, time and strength calibrated air puff stimulator that allows both tactile stimulation and sham control. We combined this with the use of event-related potential methodology to allow for high temporal resolution of signals from the primary and secondary somatosensory cortices as well as higher order processing. This methodology also allowed us to measure a multisensory response to auditory-tactile stimulation.     

Perceived Loudness of Self-Generated Sounds Is Differentially Modified by Expected Sound Intensity

Performing actions with sensory consequences modifies physiological and behavioral responses relative to otherwise identical sensory input perceived in a passive manner. It is assumed that such modifications occur through an efference copy sent from motor cortex to sensory regions during performance of voluntary actions. In the auditory domain most behavioral studies report attenuated perceived loudness of self-generated auditory action-consequences. However, several recent behavioral and physiological studies report enhanced responses to such consequences. Here we manipulated the intensity of self-generated and externally-generated sounds and examined the type of perceptual modification (enhancement vs. attenuation) reported by healthy human subjects. We found that when the intensity of self-generated sounds was low, perceived loudness is enhanced. Conversely, when the intensity of self-generated sounds was high, perceived loudness is attenuated. These results might reconcile some of the apparent discrepancies in the reported literature and suggest that efference copies can adapt perception according to the differential sensory context of voluntary actions.     

Integrating information from different senses in the auditory cortex

Multisensory integration was once thought to be the domain of brain areas high in the cortical hierarchy, with early sensory cortical fields devoted to unisensory processing of inputs from their given set of sensory receptors. More recently, a wealth of evidence documenting visual and somatosensory responses in auditory cortex, even as early as the primary fields, has changed this view of cortical processing. These multisensory inputs may serve to enhance responses to sounds that are accompanied by other sensory cues, effectively making them easier to hear, but may also act more selectively to shape the receptive field properties of auditory cortical neurons to the location or identity of these events. We discuss the new, converging evidence that multiplexing of neural signals may play a key role in informatively encoding and integrating signals in auditory cortex across multiple sensory modalities. We highlight some of the many open research questions that exist about the neural mechanisms that give rise to multisensory integration in auditory cortex, which should be addressed in future experimental and theoretical studies.     

Ontogeny of auditory saccular sensitivity in the plainfin midshipman fish, <Emphasis Type="Italic">Porichthys notatus</Emphasis>

The auditory system of the plainfin midshipman fish, Porichthys notatus, is an important sensory receiver system used to encode intraspecific social communication signals in adults, but the response properties and function of this receiver system in pre-adult stages are less known. In this study we examined the response properties of auditory-evoked potentials from the midshipman saccule, the main organ of hearing in this species, to determine whether the frequency response and auditory threshold of saccular hair cells to behaviorally relevant single tone stimuli change during ontogeny. Saccular potentials were recorded from three relative sizes of midshipman fish: small juveniles [1.9–3.1 cm standard length (SL), large juveniles (6.8–8.0 cm SL) and non-reproductive adults (9.0–22.6 cm SL)]. The auditory evoked potentials were recorded from the rostral, middle and caudal regions of the saccule while single tone stimuli (75–1,025 Hz) were presented via an underwater speaker. We show that the frequency response and auditory threshold of the midshipman saccule is established early in development and retained throughout ontogeny. We also show that saccular sensitivity to frequencies greater than 385 Hz increases with age/size and that the midshipman saccule of small and large juveniles, like that of non-reproductive adults, is best suited to detect low frequency sounds (<105 Hz) in their natural acoustic environment.     

What are you doing? How active and observational experience shape infants' action understanding

From early in life, infants watch other people''s actions. How do young infants come to make sense of actions they observe? Here, we review empirical findings on the development of action understanding in infancy. Based on this review, we argue that active action experience is crucial for infants'' developing action understanding. When infants execute actions, they form associations between motor acts and the sensory consequences of these acts. When infants subsequently observe these actions in others, they can use their motor system to predict the outcome of the ongoing actions. Also, infants come to an understanding of others’ actions through the repeated observation of actions and the effects associated with them. In their daily lives, infants have plenty of opportunities to form associations between observed events and learn about statistical regularities of others’ behaviours. We argue that based on these two forms of experience—active action experience and observational experience—infants gradually develop more complex action understanding capabilities.     

Role of bradykinin in gastric vasodilation caused by hypertonic saline and acid back diffusion

Protective vasodilation in response to tissue injury and acid back diffusion is associated with release of bradykinin in the rat stomach. We hypothesized that bradykinin might be involved in mechanisms behind such vasodilation via influence on mast cells and sensory neurons. Acid back diffusion after mucosal barrier disruption with hypertonic saline evoked degranulation of mast cells in the rat stomach wall. Acid back diffusion was also associated with increased luminal release of histamine and gastric blood flow in normal rats, but not in mast cell-deficient rats. Bradykinin (BK(2)) receptor blockade inhibited degranulation of submucosal mast cells in the stomach and attenuated gastric vasodilation both in response to acid back diffusion and after stimulation of sensory neurons with capsaicin. Gastric vasodilation caused by mucosal injury with hypertonic saline alone was associated with degranulation of mucosal mast cells. These events were unaffected by inhibition of prostaglandin synthesis, whereas bradykinin (BK(2)) receptor blockade was associated with abolished vasodilation and inhibition of mucosal mast cell degranulation. We conclude that bradykinin is involved in gastric vasodilation caused by hypertonic injury alone via influence on mast cells, and by acid back diffusion via influence on both sensory neurons and mast cells.     

Temporal Features of Spike Trains in the Moth Antennal Lobe Revealed by a Comparative Time-Frequency Analysis

The discrimination of complex sensory stimuli in a noisy environment is an immense computational task. Sensory systems often encode stimulus features in a spatiotemporal fashion through the complex firing patterns of individual neurons. To identify these temporal features, we have developed an analysis that allows the comparison of statistically significant features of spike trains localized over multiple scales of time-frequency resolution. Our approach provides an original way to utilize the discrete wavelet transform to process instantaneous rate functions derived from spike trains, and select relevant wavelet coefficients through statistical analysis. Our method uncovered localized features within olfactory projection neuron (PN) responses in the moth antennal lobe coding for the presence of an odor mixture and the concentration of single component odorants, but not for compound identities. We found that odor mixtures evoked earlier responses in biphasic response type PNs compared to single components, which led to differences in the instantaneous firing rate functions with their signal power spread across multiple frequency bands (ranging from 0 to 45.71 Hz) during a time window immediately preceding behavioral response latencies observed in insects. Odor concentrations were coded in excited response type PNs both in low frequency band differences (2.86 to 5.71 Hz) during the stimulus and in the odor trace after stimulus offset in low (0 to 2.86 Hz) and high (22.86 to 45.71 Hz) frequency bands. These high frequency differences in both types of PNs could have particular relevance for recruiting cellular activity in higher brain centers such as mushroom body Kenyon cells. In contrast, neurons in the specialized pheromone-responsive area of the moth antennal lobe exhibited few stimulus-dependent differences in temporal response features. These results provide interesting insights on early insect olfactory processing and introduce a novel comparative approach for spike train analysis applicable to a variety of neuronal data sets.     

Activity in a Premotor Cortical Nucleus of Zebra Finches Is Locally Organized and Exhibits Auditory Selectivity in Neurons but Not in Glia

Motor functions are often guided by sensory experience, most convincingly illustrated by complex learned behaviors. Key to sensory guidance in motor areas may be the structural and functional organization of sensory inputs and their evoked responses. We study sensory responses in large populations of neurons and neuron-assistive cells in the songbird motor area HVC, an auditory-vocal brain area involved in sensory learning and in adult song production. HVC spike responses to auditory stimulation display remarkable preference for the bird''s own song (BOS) compared to other stimuli. Using two-photon calcium imaging in anesthetized zebra finches we measure the spatio-temporal structure of baseline activity and of auditory evoked responses in identified populations of HVC cells. We find strong correlations between calcium signal fluctuations in nearby cells of a given type, both in identified neurons and in astroglia. In identified HVC neurons only, auditory stimulation decorrelates ongoing calcium signals, less for BOS than for other sound stimuli. Overall, calcium transients show strong preference for BOS in identified HVC neurons but not in astroglia, showing diversity in local functional organization among identified neuron and astroglia populations.     

Similarity of Cortical Activity Patterns Predicts generalization Behavior

Humans and animals readily generalize previously learned knowledge to new situations. Determining similarity is critical for assigning category membership to a novel stimulus. We tested the hypothesis that category membership is initially encoded by the similarity of the activity pattern evoked by a novel stimulus to the patterns from known categories. We provide behavioral and neurophysiological evidence that activity patterns in primary auditory cortex contain sufficient information to explain behavioral categorization of novel speech sounds by rats. Our results suggest that category membership might be encoded by the similarity of the activity pattern evoked by a novel speech sound to the patterns evoked by known sounds. Categorization based on featureless pattern matching may represent a general neural mechanism for ensuring accurate generalization across sensory and cognitive systems.     

Brain mechanisms associated with top-down processes in perception.

Perception arises through an interaction between sensory input and prior knowledge. We propose that at least two brain areas are required for such an interaction: the ''site'' where analysis of afferent signals occurs and the ''source'' which applies the relevant prior knowledge. In the human brain, functional imaging studies have demonstrated that selective attention modifies activity in early visual processing areas specific to the attended feature. Early processing areas are also modified when prior knowledge permits a percept to emerge from an otherwise meaningless stimulus. Sources of this modification have been identified in parietal cortex and in prefrontal cortex. Modification of early processing areas also occurs on the basis of prior knowledge about the predicted sensory effects of the subject''s own actions. Activity associated with mental imagery resembles that associated with response preparation (for motor imagery) and selective attention (for sensory imagery) suggesting that mental imagery reflects the effects of prior knowledge on sensory processing areas in the absence of sensory input. Damage to sensory processing areas can lead to a form of sensory hallucination which seems to arise from the interaction of prior knowledge with random sensory activity. In contrast, hallucinations associated with schizophrenia may arise from a failure of prior knowledge about motor intentions to modify activity in relevant sensory areas. When functioning normally, this mechanism permits us to distinguish our own actions from those of independent agents in the outside world. Failure to make this distinction correctly may account for the strong association between hallucinations and paranoid delusions in schizophrenia; the patient not only hears voices, but attributes (usually hostile) intentions to these voices.