Developmental, functional brain imaging and electrophysiological evidence of visual and auditory working memory

Intact function of working memory (WM) is essential for children and adults to cope with every day life. Children with deficits in WM mechanisms have learning difficulties that are often accompanied by behavioral problems. The neural processes subserving WM, and brain structures underlying this system, continue to develop during childhood till adolescence and young adulthood. With functional magnetic resonance imaging (fMRI) it is possible to investigate the organization and development of WM. The present thesis aimed to investigate, using behavioral and neuroimaging methods, whether mnemonic processing of spatial and nonspatial visual information is segregated in the developing and mature human brain. A further aim in this research was to investigate the organization and development of audiospatial and visuospatial information processing in WM. The behavioral results showed that spatial and nonspatial visual WM processing is segregated in the adult brain. The fMRI result in children suggested that memory load related processing of spatial and nonspatial visual information engages common cortical networks, whereas selective attention to either type of stimuli recruits partially segregated areas in the frontal, parietal and occipital cortices. Deactivation mechanisms that are important in the performance of WM tasks in adults are already operational in healthy school-aged children. Electrophysiological evidence suggested segregated mnemonic processing of visual and auditory location information. The results of the development of audiospatial and visuospatial WM demonstrate that WM performance improves with age, suggesting functional maturation of underlying cognitive processes and brain areas. The development of the performance of spatial WM tasks follows a different time course in boys and girls indicating a larger degree of immaturity in the male than female WM systems. Furthermore, the differences in mastering auditory and visual WM tasks may indicate that visual WM reaches functional maturity earlier than the corresponding auditory system. Spatial WM deficits may underlie some learning difficulties and behavioral problems related to impulsivity, difficulties in concentration, and hyperactivity. Alternatively, anxiety or depressive symptoms may affect WM function and the ability to concentrate, being thus the primary cause of poor academic achievement in children.

Tactile processing in human somatosensory and auditory cortices

Tactile sensation plays an important role in everyday life. While the somatosensory system has been studied extensively, the majority of information has come from studies using animal models. Recent development of high-resolution anatomical and functional imaging techniques has enabled the non-invasive study of human somatosensory cortex and thalamus. This thesis provides new insights into the functional organization of the human brain areas involved in tactile processing using magnetoencephalography (MEG) and functional magnetic resonance imaging (fMRI). The thesis also demonstrates certain optimizations of MEG and fMRI methods. Tactile digit stimulation elicited stimulus-specific responses in a number of brain areas. Contralateral activation was observed in somatosensory thalamus (Study II), primary somatosensory cortex (SI; I, III, IV), and post-auditory belt area (III). Bilateral activation was observed in secondary somatosensory cortex (SII; II, III, IV). Ipsilateral activation was found in the post-central gyrus (area 2 of SI cortex; IV). In addition, phasic deactivation was observed within ipsilateral SI cortex and bilateral primary motor cortex (IV). Detailed investigation of the tactile responses demonstrated that the arrangement of distal-proximal finger representations in area 3b of SI in humans is similar to that found in monkeys (I). An optimized MEG approach was sufficient to resolve such fine detail in functional organization. The SII region appeared to contain double representations for fingers and toes (II). The detection of activations in the SII region and thalamus improved at the individual and group levels when cardiac-gated fMRI was used (II). Better detection of body part representations at the individual level is an important improvement, because identification of individual representations is crucial for studying brain plasticity in somatosensory areas. The posterior auditory belt area demonstrated responses to both auditory and tactile stimuli (III), implicating this area as a physiological substrate for the auditory-tactile interaction observed in earlier psychophysical studies. Comparison of different smoothing parameters (III) demonstrated that proper evaluation of co-activation should be based on individual subject analysis with minimal or no smoothing. Tactile input consistently influenced area 3b of the human ipsilateral SI cortex (IV). The observed phasic negative fMRI response is proposed to result from interhemispheric inhibition via trans-callosal connections. This thesis contributes to a growing body of human data suggesting that processing of tactile stimuli involves multiple brain areas, with different spatial patterns of cortical activation for different stimuli.

Binaural Localization and Masking

Binaural experiments are described which indicate that the ability of the brain to localize a desired sound and to suppress undesired sounds coming from other directions can be traced in part to the different times of arrival of a sound at the two ears. It is suggested that the brain inserts a time delay in one of the two nerve paths associated with the ears so as to be able to compare, and thus concentrate on, those sounds arriving at the ears with this particular time of arrival distance.The ability to perceive weak sounds binaurally in the presence of noise is shown to be a simple function of the direction of the desired sound and noise. An explanation is given for the effect reported by Koenig that front and rear confusion is avoided by head movements.

Task-dependent activations of human auditory cortex during pitch discrimination and pitch memory tasks

"The functional organization of auditory cortex (AC) is still poorly understood. Previous studies suggest segregation of auditory processing streams for spatial and nonspatial information located in the posterior and anterior AC, respectively (Rauschecker and Tian, 2000; Arnott et al., 2004; Lomber and Malhotra, 2008). Furthermore, previous studies have shown that active listening tasks strongly modulate AC activations (Petkov et al., 2004; Fritz et al., 2005; Polley et al., 2006). However, the task dependence of AC activations has not been systematically investigated. In the present study, we applied high-resolution functional magnetic resonance imaging of the AC and adjacent areas to compare activations during pitch discrimination and n-back pitch memory tasks that were varied parametrically in difficulty. We found that anterior AC activations were increased during discrimination but not during memory tasks, while activations in the inferior parietal lobule posterior to the AC were enhanced during memory tasks but not during discrimination. We also found that wide areas of the anterior AC and anterior insula were strongly deactivated during the pitch memory tasks. While these results are consistent with the proposition that the anterior and posterior AC belong to functionally separate auditory processing streams, our results show that this division is present also between tasks using spatially invariant sounds. Together, our results indicate that activations of human AC are strongly dependent on the characteristics of the behavioral task."

Towards Optimal Testing of Auditory Memory : Methodological development of recording of the mismatch negativity (MMN) of the auditory event-related potential (ERP)

The overlapping sound pressure waves that enter our brain via the ears and auditory nerves must be organized into a coherent percept. Modelling the regularities of the auditory environment and detecting unexpected changes in these regularities, even in the absence of attention, is a necessary prerequisite for orientating towards significant information as well as speech perception and communication, for instance. The processing of auditory information, in particular the detection of changes in the regularities of the auditory input, gives rise to neural activity in the brain that is seen as a mismatch negativity (MMN) response of the event-related potential (ERP) recorded by electroencephalography (EEG). --- As the recording of MMN requires neither a subject s behavioural response nor attention towards the sounds, it can be done even with subjects with problems in communicating or difficulties in performing a discrimination task, for example, from aphasic and comatose patients, newborns, and even fetuses. Thus with MMN one can follow the evolution of central auditory processing from the very early, often critical stages of development, and also in subjects who cannot be examined with the more traditional behavioural measures of auditory discrimination. Indeed, recent studies show that central auditory processing, as indicated by MMN, is affected in different clinical populations, such as schizophrenics, as well as during normal aging and abnormal childhood development. Moreover, the processing of auditory information can be selectively impaired for certain auditory attributes (e.g., sound duration, frequency) and can also depend on the context of the sound changes (e.g., speech or non-speech). Although its advantages over behavioral measures are undeniable, a major obstacle to the larger-scale routine use of the MMN method, especially in clinical settings, is the relatively long duration of its measurement. Typically, approximately 15 minutes of recording time is needed for measuring the MMN for a single auditory attribute. Recording a complete central auditory processing profile consisting of several auditory attributes would thus require from one hour to several hours. In this research, I have contributed to the development of new fast multi-attribute MMN recording paradigms in which several types and magnitudes of sound changes are presented in both speech and non-speech contexts in order to obtain a comprehensive profile of auditory sensory memory and discrimination accuracy in a short measurement time (altogether approximately 15 min for 5 auditory attributes). The speed of the paradigms makes them highly attractive for clinical research, their reliability brings fidelity to longitudinal studies, and the language context is especially suitable for studies on language impairments such as dyslexia and aphasia. In addition I have presented an even more ecological paradigm, and more importantly, an interesting result in view of the theory of MMN where the MMN responses are recorded entirely without a repetitive standard tone. All in all, these paradigms contribute to the development of the theory of auditory perception, and increase the feasibility of MMN recordings in both basic and clinical research. Moreover, they have already proven useful in studying for instance dyslexia, Asperger syndrome and schizophrenia.

Novel auditory motivated subband temporal envelope based fundamental frequency estimation algorithm

We address the problem of estimating the fundamental frequency of voiced speech. We present a novel solution motivated by the importance of amplitude modulation in sound processing and speech perception. The new algorithm is based on a cumulative spectrum computed from the temporal envelope of various subbands. We provide theoretical analysis to derive the new pitch estimator based on the temporal envelope of the bandpass speech signal. We report extensive experimental performance for synthetic as well as natural vowels for both realworld noisy and noise-free data. Experimental results show that the new technique performs accurate pitch estimation and is robust to noise. We also show that the technique is superior to the autocorrelation technique for pitch estimation.

Auditory-motivated Gammatone wavelet transform

The ability of the continuous wavelet transform (CWT) to provide good time and frequency localization has made it a popular tool in time-frequency analysis of signals. Wavelets exhibit constant-Q property, which is also possessed by the basilar membrane filters in the peripheral auditory system. The basilar membrane filters or auditory filters are often modeled by a Gammatone function, which provides a good approximation to experimentally determined responses. The filterbank derived from these filters is referred to as a Gammatone filterbank. In general, wavelet analysis can be likened to a filterbank analysis and hence the interesting link between standard wavelet analysis and Gammatone filterbank. However, the Gammatone function does not exactly qualify as a wavelet because its time average is not zero. We show how bona fide wavelets can be constructed out of Gammatone functions. We analyze properties such as admissibility, time-bandwidth product, vanishing moments, which are particularly relevant in the context of wavelets. We also show how the proposed auditory wavelets are produced as the impulse response of a linear, shift-invariant system governed by a linear differential equation with constant coefficients. We propose analog circuit implementations of the proposed CWT. We also show how the Gammatone-derived wavelets can be used for singularity detection and time-frequency analysis of transient signals. (C) 2013 Elsevier B.V. All rights reserved.

Modelling the effects of chorus species composition and caller density on acoustic masking interference in multispecies choruses of crickets and katydids

Natural multispecies acoustic choruses such as the dusk chorus of a tropical rain forest consist of simultaneously signalling individuals of different species whose calls travel through a common shared medium before reaching their `intended' receivers. This causes masking interference between signals and impedes signal detection, recognition and localization. The levels of acoustic overlap depend on a number of factors, including call structure, intensity, habitat-dependent signal attenuation and receiver tuning. In addition, acoustic overlaps should also depend on caller density and the species composition of choruses, including relative and absolute abundance of the different calling species. In this study, we used simulations to examine the effects of chorus species relative abundance and caller density on the levels of effective heterospecific acoustic overlap in multispecies choruses composed of the calls of five species of crickets and katydids that share the understorey of a rain forest in southern India. We found that on average species-even choruses resulted in higher levels of effective heterospecific acoustic overlap than choruses with strong dominance structures. This effect was found consistently across dominance levels ranging from 0.4 to 0.8 for larger choruses of forty individuals. For smaller choruses of twenty individuals, the effect was seen consistently for dominance levels of 0.6 and 0.8 but not 0.4. Effective acoustic overlap (EAO) increased with caller density but the manner and extent of increase depended both on the species' call structure and the acoustic context provided by the composition scenario. The Phaloria sp. experienced very low levels of EAO and was highly buffered to changes in acoustic context whereas other species experienced high FAO across contexts or were poorly buffered. These differences were not simply predictable from call structures. These simulation-based findings may have important implications for acoustic biodiversity monitoring and for the study of acoustic masking interference in natural environments. (C) 2013 Elsevier B.V. All rights reserved.

Ecology of acoustic signalling and the problem of masking interference in insects

The efficiency of long-distance acoustic signalling of insects in their natural habitat is constrained in several ways. Acoustic signals are not only subjected to changes imposed by the physical structure of the habitat such as attenuation and degradation but also to masking interference from co-occurring signals of other acoustically communicating species. Masking interference is likely to be a ubiquitous problem in multi-species assemblages, but successful communication in natural environments under noisy conditions suggests powerful strategies to deal with the detection and recognition of relevant signals. In this review we present recent work on the role of the habitat as a driving force in shaping insect signal structures. In the context of acoustic masking interference, we discuss the ecological niche concept and examine the role of acoustic resource partitioning in the temporal, spatial and spectral domains as sender strategies to counter masking. We then examine the efficacy of different receiver strategies: physiological mechanisms such as frequency tuning, spatial release from masking and gain control as useful strategies to counteract acoustic masking. We also review recent work on the effects of anthropogenic noise on insect acoustic communication and the importance of insect sounds as indicators of biodiversity and ecosystem health.

Neural representation of auditory temporal structure

Neurons in the songbird forebrain nucleus HVc are highly sensitive to auditory temporal context and have some of the most complex auditory tuning properties yet discovered. HVc is crucial for learning, perceiving, and producing song, thus it is important to understand the neural circuitry and mechanisms that give rise to these remarkable auditory response properties. This thesis investigates these issues experimentally and computationally.

Extracellular studies reported here compare the auditory context sensitivity of neurons in HV c with neurons in the afferent areas of field L. These demonstrate that there is a substantial increase in the auditory temporal context sensitivity from the areas of field L to HVc. Whole-cell recordings of HVc neurons from acute brain slices are described which show that excitatory synaptic transmission between HVc neurons involve the release of glutamate and the activation of both AMPA/kainate and NMDA-type glutamate receptors. Additionally, widespread inhibitory interactions exist between HVc neurons that are mediated by postsynaptic GABA_A receptors. Intracellular recordings of HVc auditory neurons in vivo provides evidence that HV c neurons encode information about temporal structure using a variety of cellular and synaptic mechanisms including syllable-specific inhibition, excitatory post-synaptic potentials with a range of different time courses, and burst-firing, and song-specific hyperpolarization.

The final part of this thesis presents two computational approaches for representing and learning temporal structure. The first method utilizes comput ational elements that are analogous to temporal combination sensitive neurons in HVc. A network of these elements can learn using local information and lateral inhibition. The second method presents a more general framework which allows a network to discover mixtures of temporal features in a continuous stream of input.

Responses to auditory stimuli in macaque lateral intraparietal area

The lateral intraparietal area (LIP) of macaque posterior parietal cortex participates in the sensorimotor transformations underlying visually guided eye movements. Area LIP has long been considered unresponsive to auditory stimulation. However, recent studies have shown that neurons in LIP respond to auditory stimuli during an auditory-saccade task, suggesting possible involvement of this area in auditory-to-oculomotor as well as visual-to-oculomotor processing. This dissertation describes investigations which clarify the role of area LIP in auditory-to-oculomotor processing.

Extracellular recordings were obtained from a total of 332 LIP neurons in two macaque monkeys, while the animals performed fixation and saccade tasks involving auditory and visual stimuli. No auditory activity was observed in area LIP before animals were trained to make saccades to auditory stimuli, but responses to auditory stimuli did emerge after auditory-saccade training. Auditory responses in area LIP after auditory-saccade training were significantly stronger in the context of an auditory-saccade task than in the context of a fixation task. Compared to visual responses, auditory responses were also significantly more predictive of movement-related activity in the saccade task. Moreover, while visual responses often had a fast transient component, responses to auditory stimuli in area LIP tended to be gradual in onset and relatively prolonged in duration.

Overall, the analyses demonstrate that responses to auditory stimuli in area LIP are dependent on auditory-saccade training, modulated by behavioral context, and characterized by slow-onset, sustained response profiles. These findings suggest that responses to auditory stimuli are best interpreted as supramodal (cognitive or motor) responses, rather than as modality-specific sensory responses. Auditory responses in area LIP seem to reflect the significance of auditory stimuli as potential targets for eye movements, and may differ from most visual responses in the extent to which they arc abstracted from the sensory parameters of the stimulus.