Spatial and cross-modal attention alter responses to unattended sensory information in early visual and auditory human cortex

Attending to a visual or auditory stimulus often requires irrelevant information to be filtered out, both within the modality attended and in other modalities. For example, attentively listening to a phone conversation can diminish our ability to detect visual events. We used functional magnetic resonance imaging (fMRI) to examine brain responses to visual and auditory stimuli while subjects attended visual or auditory information. Although early cortical areas are traditionally considered unimodal, we found that brain responses to the same ignored information depended on the modality attended. In early visual area V1, responses to ignored visual stimuli were weaker when attending to another visual stimulus, compared with attending to an auditory stimulus. The opposite was true in more central visual area MT+, where responses to ignored visual stimuli were weaker when attending to an auditory stimulus. Furthermore, fMRI responses to the same ignored visual information depended on the location of the auditory stimulus, with stronger responses when the attended auditory stimulus shared the same side of space as the ignored visual stimulus. In early auditory cortex, responses to ignored auditory stimuli were weaker when attending a visual stimulus. A simple parameterization of our data can describe the effects of redirecting attention across space within the same modality (spatial attention) or across modalities (cross-modal attention), and the influence of spatial attention across modalities (cross-modal spatial attention). Our results suggest that the representation of unattended information depends on whether attention is directed to another stimulus in the same modality or the same region of space.     

Absence of cross-modal reorganization in the primary auditory cortex of congenitally deaf cats

To investigate possible cross-modal reorganization of the primary auditory cortex (field A1) in congenitally deaf cats, after years of auditory deprivation, multiunit activity and local field potentials were recorded in lightly anesthetized animals and compared with responses obtained in hearing cats. Local field potentials were also used for current source-density analyses. For visual stimulation, phase-reversal gratings of three to five different spatial frequencies and three to five different orientations were presented at the point of central vision. Peripheral visual field was tested using hand-held stimuli (light bar-shaped stimulus of different orientations, moved in different directions and flashed) typically used for neurophysiological characterization of visual fields. From 200 multiunit recordings, no response to visual stimuli could be found in A1 of any of the investigated animals. Using the current source-density analysis of local field potentials, no local generators of field potentials could be found within A1, despite of the presence of small local field potentials. No multiunit responses to somatosensory stimulation (whiskers, face, pinna, head, neck, all paws, back, tail) could be obtained. In conclusion, there were no indications for a cross-modal reorganization (visual, somatosensory) of area A1 in congenitally deaf cats.     

GABA concentrations in the human anterior cingulate cortex predict negative BOLD responses in fMRI

The human anterior cingulate cortex (ACC) is part of the default-mode network that shows predominant negative blood oxygen level-dependent (BOLD) responses in functional magnetic resonance imaging (fMRI). We combined fMRI during emotional processing and resting-state magnetic resonance spectroscopy measurements and observed that the concentration of GABA in the ACC specifically correlated with the amount of negative BOLD responses in the very same region. Our findings show that default-mode network negative BOLD responses during emotions are mediated by GABA.     

Auditory-somatosensory multisensory processing in auditory association cortex: an fMRI study

Using high-field (3 Tesla) functional magnetic resonance imaging (fMRI), we demonstrate that auditory and somatosensory inputs converge in a subregion of human auditory cortex along the superior temporal gyrus. Further, simultaneous stimulation in both sensory modalities resulted in activity exceeding that predicted by summing the responses to the unisensory inputs, thereby showing multisensory integration in this convergence region. Recently, intracranial recordings in macaque monkeys have shown similar auditory-somatosensory convergence in a subregion of auditory cortex directly caudomedial to primary auditory cortex (area CM). The multisensory region identified in the present investigation may be the human homologue of CM. Our finding of auditory-somatosensory convergence in early auditory cortices contributes to mounting evidence for multisensory integration early in the cortical processing hierarchy, in brain regions that were previously assumed to be unisensory.     

Spatial sensitivity in field PAF of cat auditory cortex

We compared the spatial tuning properties of neurons in two fields [primary auditory cortex (A1) and posterior auditory field (PAF)] of cat auditory cortex. Broadband noise bursts of 80-ms duration were presented from loudspeakers throughout 360 degrees in the horizontal plane (azimuth) or 260 degrees in the vertical median plane (elevation). Sound levels varied from 20 to 40 dB above units' thresholds. We recorded neural spike activity simultaneously from 16 sites in field PAF and/or A1 of alpha-chloralose-anesthetized cats. We assessed spatial sensitivity by examining the dependence of spike count and response latency on stimulus location. In addition, we used an artificial neural network (ANN) to assess the information about stimulus location carried by spike patterns of single units and of ensembles of 2-32 units. The results indicate increased spatial sensitivity, more uniform distributions of preferred locations, and greater tolerance to changes in stimulus intensity among PAF units relative to A1 units. Compared to A1 units, PAF units responded at significantly longer latencies, and latencies varied more strongly with stimulus location. ANN analysis revealed significantly greater information transmission by spike patterns of PAF than A1 units, primarily reflecting the information transmitted by latency variation in PAF. Finally, information rates grew more rapidly with the number of units included in neural ensembles for PAF than A1. The latter finding suggests more accurate population coding of space in PAF, made possible by a more diverse population of neural response types.     

BOLD fMRI identifies limbic,paralimbic, and cerebellar activation during air hunger

Air hunger (uncomfortable urge to breathe) is a component of dyspnea (shortness of breath). Three human H(2)(15)O positron emission tomography (PET) studies have identified activation of phylogenetically ancient structures in limbic and paralimbic regions during dyspnea. Other studies have shown activation of these structures during other sensations that alert the organism to urgent homeostatic imbalance: pain, thirst, and hunger for food. We employed blood oxygen level dependent (BOLD) functional magnetic resonance imaging (fMRI) to examine activation during air hunger. fMRI conferred several advantages over PET: enhanced signal-to-noise, greater spatial resolution, and lack of ionizing radiation, enabling a greater number of trials in each subject. Six healthy men and women were mechanically ventilated at 12-14 breaths/min. The primary experiment was conducted at mean end-tidal PCO(2) of 41 Torr. Moderate to severe air hunger was evoked during 42-s epochs of lower tidal volume (mean = 0.75 L). Subjects described the sensation as "like breath-hold," "urge to breathe," and "starved for air." In the baseline condition, air hunger was consistently relieved by epochs of higher tidal volume (mean = 1.47 L). A control experiment in the same subjects under a background of mild hypocapnia (mean end-tidal PCO(2) = 33 Torr) employed similar tidal volumes but did not evoke air hunger, controlling for stimulus variables not related to dyspnea. During each experiment, we maintained constant end-tidal PCO(2) and PO(2) to avoid systematic changes in global cerebral blood flow. Whole-brain images were acquired every 5 s (T2*, 56 slices, voxel resolution 3 x 3 x 3 mm). Activations associated with air hunger were determined using voxel-based interaction analysis of covariance that compared data between primary and control experiments (SPM99). We detected activations not seen in the earlier PET study using a similar air hunger stimulus (Banzett et al. 2000). Limbic and paralimbic loci activated in the present study were within anterior insula (seen in all 3 published studies of dyspnea), anterior cingulate, operculum, cerebellum, amygdala, thalamus, and basal ganglia. Elements of frontoparietal attentional networks were also identified. The consistency of anterior insular activation across subjects in this study and across published studies suggests that the insula is essential to dyspnea perception, although present data suggest that the insula acts in concert with a larger neural network.     

Segregation of somatosensory activation in the human rolandic cortex using fMRI

The segregation of sensory information into distinct cortical areas is an important organizational feature of mammalian sensory systems. Here, we provide functional magnetic resonance imaging (fMRI) evidence for the functional delineation of somatosensory representations in the human central sulcus region. Data were collected with a 3-Tesla scanner during two stimulation protocols, a punctate tactile condition without a kinesthetic/motor component, and a kinesthetic/motor condition without a punctate tactile component. With three-dimensional (3-D) anatomical reconstruction techniques, we analyzed data in individual subjects, using the pattern of activation and the anatomical position of specific cortical areas to guide the analysis. As a complimentary analysis, we used a brain averaging technique that emphasized the similarity of cortical features in the morphing of individual subjects and thereby minimized the distortion of the location of cortical activation sites across individuals. A primary finding of this study was differential activation of the cortex on the fundus of the central sulcus, the position of area 3a, during the two tasks. Punctate tactile stimulation of the palm, administered at 3 Hz with a 5.88(log10.mg) von Frey filament, activated discrete regions within the precentral (PreCG) and postcentral (PoCG) gyri, corresponding to areas 6, 3b, 1, and 2, but did not activate area 3a. Conversely, kinesthetic/motor stimulation, 3-Hz flexion and extension of the digits, activated area 3a, the PreCG (areas 6 and 4), and the PoCG (areas 3b, 1, and 2). These activation patterns were observed in individual subjects and in the averaged data, providing strong evidence for the existence of a distinct representation within area 3a in humans. The percentage signal changes in the PreCG and PoCG regions activated by tactile stimulation, and in the intervening gap region, support this functional dissociation. In addition to this distinction within the fundus of the central sulcus, the combination of high-resolution imaging and 3-D analysis techniques permitted localization of activation within areas 6, 4, 3a, 3b, 1, and 2 in the human. With the exception of area 4, which showed inconsistent activation during punctate tactile stimulation, activation in these areas in the human consistently paralleled the pattern of activity observed in previous studies of monkey cortex.     

Neural coding of temporal information in auditory thalamus and cortex

How the brain processes temporal information embedded in sounds is a core question in auditory research. This article synthesizes recent studies from our laboratory regarding neural representations of time-varying signals in auditory cortex and thalamus in awake marmoset monkeys. Findings from these studies show that 1) the primary auditory cortex (A1) uses a temporal representation to encode slowly varying acoustic signals and a firing rate–based representation to encode rapidly changing acoustic signals, 2) the dual temporal-rate representations in A1 represent a progressive transformation from the auditory thalamus, 3) firing rate–based representations in the form of a monotonic rate-code are also found to encode slow temporal repetitions in the range of acoustic flutter in A1 and more prevalently in the cortical fields rostral to A1 in the core region of marmoset auditory cortex, suggesting further temporal-to-rate transformations in higher cortical areas. These findings indicate that the auditory cortex forms internal representations of temporal characteristics of sounds that are no longer faithful replicas of their acoustic structures. We suggest that such transformations are necessary for the auditory cortex to perform a wide range of functions including sound segmentation, object processing and multi-sensory integration.     

Neural coding of temporal information in auditory thalamus and cortex

How the brain processes temporal information embedded in sounds is a core question in auditory research. This article synthesizes recent studies from our laboratory regarding neural representations of time-varying signals in auditory cortex and thalamus in awake marmoset monkeys. Findings from these studies show that 1) the primary auditory cortex (A1) uses a temporal representation to encode slowly varying acoustic signals and a firing rate-based representation to encode rapidly changing acoustic signals, 2) the dual temporal-rate representations in A1 represent a progressive transformation from the auditory thalamus, 3) firing rate-based representations in the form of monotonic rate-code are also found to encode slow temporal repetitions in the range of acoustic flutter in A1 and more prevalently in the cortical fields rostral to A1 in the core region of marmoset auditory cortex, suggesting further temporal-to-rate transformations in higher cortical areas. These findings indicate that the auditory cortex forms internal representations of temporal characteristics of sounds that are no longer faithful replicas of their acoustic structures. We suggest that such transformations are necessary for the auditory cortex to perform a wide range of functions including sound segmentation, object processing and multi-sensory integration.     

Plasticity of temporal information processing in the primary auditory cortex

Neurons in the rat primary auditory cortex (A1) generally cannot respond to tone sequences faster than 12 pulses per second (pps). To test whether experience can modify this maximum following rate in adult rats, trains of brief tones with random carrier frequency but fixed repetition rate were paired with electrical stimulation of the nucleus basalis (NB) 300 to 400 times per day for 20-25 days. Pairing NB stimulation with 5-pps stimuli markedly decreased the cortical response to rapidly presented stimuli, whereas pairing with 15-pps stimuli significantly increased the maximum cortical following rate. In contrast, pairing with fixed carrier frequency 15-pps trains did not significantly increase the mean maximum following rate. Thus this protocol elicits extensive cortical remodeling of temporal response properties and demonstrates that simple differences in spectral and temporal features of the sensory input can drive very different cortical reorganizations.     

A Study on Asymmetry of Spatial Visual Field by Analysis of the fMRI BOLD Response

The asymmetry of the left-right and upper-lower visual field is analyzed in this paper by a model approach based on the functional magnetic resonance imaging (fMRI) blood oxygenation level dependent (BOLD) response. The model consists of the convolution between a Gaussian function and the perfusion function of neural response to stimulus. The model parameters are estimated by a nonlinear optimal algorithm, and te asymmetry of the left-right and upper-lower visual field is investigated by the differences of the model parameters. The results from eight subjects show that reaction time is significant shorter and the response is significant stronger when the lower field is stimulated than that when the upper field is stimulated. For the left and right fields, the response is different. These results provide the fMRI BOLD response evidence of the asymmetry of spatial visual fields.     

Multisensory processing in "unimodal" neurons: cross-modal subthreshold auditory effects in cat extrastriate visual cortex

Historically, the study of multisensory processing has examined the function of the definitive neuron type, the bimodal neuron. These neurons are excited by inputs from more than one sensory modality, and when multisensory stimuli are present, they can integrate their responses in a predictable manner. However, recent studies have revealed that multisensory processing in the cortex is not restricted to bimodal neurons. The present investigation sought to examine the potential for multisensory processing in nonbimodal (unimodal) neurons in the retinotopically organized posterolateral lateral suprasylvian (PLLS) area of the cat. Standard extracellular recordings were used to measure responses of all neurons encountered to both separate- and combined-modality stimulation. Whereas bimodal neurons behaved as predicted, the surprising result was that 16% of unimodal visual neurons encountered were significantly facilitated by auditory stimuli. Because these unimodal visual neurons did not respond to an auditory stimulus presented alone but had their visual responses modulated by concurrent auditory stimulation, they represent a new form of multisensory neuron: the subthreshold multisensory neuron. These data also demonstrate that bimodal neurons can no longer be regarded as the exclusive basis for multisensory processing.     

Attention differentially modulates the coupling of fMRI BOLD and evoked potential signal amplitudes in the human somatosensory cortex

Blood oxygenation dependent contrast (BOLD) fMRI is used increasingly to probe connectivity based on temporal correlations between signals from different brain regions. This approach assumes that there is constant local coupling of neuronal activity to the associated BOLD response. Here we test the alternative hypothesis that there is not a fixed relationship between these by determining whether attention modulates apparent neurovascular coupling. Electrical stimulation of the median nerve was applied with and without a concurrent distractor task (serial subtraction). Increasing stimulation intensity increased discomfort ratings (p<0.001) and was associated with a significant increase in both somatosensory evoked potential (SEP) N20-P25 amplitude and BOLD fMRI response in the contralateral primary (SI) and bilaterally in the secondary somatosensory cortices. Attention to stimulation was reduced during distractor task performance and resulted in an overall trend for reduction in discomfort (p=0.056), which was significant at the highest stimulation level (p<0.05). A volume of interest analysis confined to SI confirmed a reduction in BOLD response with distraction (p<0.001). However, distraction did not measurably affect SEP magnitude. The quantitative relationship between the BOLD fMRI response and the local field potential measured by the early SEP response therefore varies with attentional context. This may be a consequence of differences in either local spatial or temporal signal summation for the two methods. Either interpretation suggests caution in assuming a simple, fixed relationship between local BOLD changes and related electrophysiological activity.O.J. Arthurs and H. Johansen-Berg contributed equally to this work.This paper is dedicated to the memory of Dr. Simon Boniface, who died in November 2003. He will be sorely missed.     

Antidromic activation reveals tonotopically organized projections from primary auditory cortex to the central nucleus of the inferior colliculus in guinea pig

The inferior colliculus (IC) is highly modulated by descending projections from higher auditory and nonauditory centers. Traditionally, corticofugal fibers were believed to project mainly to the extralemniscal IC regions. However, there is some anatomical evidence suggesting that a substantial number of fibers from the primary auditory cortex (A1) project into the IC central nucleus (ICC) and appear to be tonotopically organized. In this study, we used antidromic stimulation combined with other electrophysiological techniques to further investigate the spatial organization of descending fibers from A1 to the ICC in ketamine-anesthetized guinea pigs. Based on our findings, corticofugal fibers originate predominantly from layer V of A1, are amply scattered throughout the ICC and only project to ICC neurons with a similar best frequency (BF). This strict tonotopic pattern suggests that these corticofugal projections are involved with modulating spectral features of sound. Along the isofrequency dimension of the ICC, there appears to be some differences in projection patterns that depend on BF region and possibly isofrequency location within A1 and may be indicative of different descending coding strategies. Furthermore, the success of the antidromic stimulation method in our study demonstrates that it can be used to investigate some of the functional properties associated with corticofugal projections to the ICC as well as to other regions (e.g., medial geniculate body, cochlear nucleus). Such a method can address some of the limitations with current anatomical techniques for studying the auditory corticofugal system.     

Sound-level-dependent representation of frequency modulations in human auditory cortex: a low-noise fMRI study.

Recognition of sound patterns must be largely independent of level and of masking or jamming background sounds. Auditory patterns of relevance in numerous environmental sounds, species-specific vocalizations and speech are frequency modulations (FM). Level-dependent activation of the human auditory cortex (AC) in response to a large set of upward and downward FM tones was studied with low-noise (48 dB) functional magnetic resonance imaging at 3 Tesla. Separate analysis in four territories of AC was performed in each individual brain using a combination of anatomical landmarks and spatial activation criteria for their distinction. Activation of territory T1b (including primary AC) showed the most robust level dependence over the large range of 48-102 dB in terms of activated volume and blood oxygen level dependent contrast (BOLD) signal intensity. The left nonprimary territory T2 also showed a good correlation of level with activated volume but, in contrast to T1b, not with BOLD signal intensity. These findings are compatible with level coding mechanisms observed in animal AC. A systematic increase of activation with level was not observed for T1a (anterior of Heschl's gyrus) and T3 (on the planum temporale). Thus these areas might not be specifically involved in processing of the overall intensity of FM. The rostral territory T1a of the left hemisphere exhibited highest activation when the FM sound level fell 12 dB below scanner noise. This supports the previously suggested special involvement of this territory in foreground-background decomposition tasks. Overall, AC of the left hemisphere showed a stronger level-dependence of signal intensity and activated volume than the right hemisphere. But any side differences of signal intensity at given levels were lateralized to right AC. This might point to an involvement of the right hemisphere in more specific aspects of FM processing than level coding.     

Contra- and ipsilateral auditory stimuli produce different activation patterns at the human auditory cortex

Auditory evoked magnetic fields were recorded over the right hemisphere of healthy humans The stimuli were noise bursts presented either to the contra- (C) or ipsilateral (I) ear in different combinations. The largest deflection of the responses, N100m (magnetic counterpart of electric N100), showed a field pattern which suggests activation of the supratemporal auditory cortex. In an oddball paradigm, where the standards (90%) were 400-ms noise bursts presented to the contralateral ear, and the deviants (10%) similar stimuli to the ipsilateral ear, the deviants elicited on the average 130% stronger equivalent dipoles for N100m than standards. Contralateral standards did not substantially decrease the response amplitude of ipsilateral deviants as compared with the response amplitude to ipsilateral stimuli alone presented at the interstimulus interval of the deviants. When two 50 ms noise bursts, separated by 310 ms, were presented once every 2 s, N100m evoked by the second stimulus of the pair was smaller when the stimuli were presented monaurally (C-C, or I-I) than to different ears (I-C or C-I). The results suggest that contra- and ipsilateral auditory stimuli are analyzed, at least in part, in different neural networks at the human auditory cortex.     

Processing of auditory and visual location information in the monkey prefrontal cortex

Visuospatial working memory mechanisms have been studied extensively at single cell level in the dorsolateral prefrontal cortex (PFCd) in nonhuman primates. Despite the importance of short-term memory of sound location for behavioral orientation, there are only a few studies on auditory spatial working memory. The purpose of this study was to investigate neuronal mechanisms underlying working memory processing of auditory and visual location information at single cell level in the PFCd. Neuronal activity was recorded in monkeys performing a delayed matching-to-sample task (DMTS). The location of a visual or auditory stimulus was used as a memorandum. The majority of the neurons that were activated during presentation of the cue memorandum were selective either for visual or auditory spatial information. A small group of cue related bimodal neurons were sensitive to the location of the cue regardless of whether the stimulus was visual or auditory, suggesting modality independent processing of spatial information at cellular level in the PFCd. Most neurons that were activated during the delay period were modality specific, responding either during visual or auditory trials. All bimodal delay related neurons that responded during both visual and auditory trials were spatially nonselective. The results of the present study suggest that in addition to the modality specific parallel mechanism, working memory of auditory and visual space also involves modality independent processing at cellular level in the PFCd.     

Emotional arousal and activation of the visual cortex: An fMRI analysis

Functional activity in the visual cortex was assessed using functional magnetic resonance imaging technology while participants viewed a series of pleasant, neutral, or unpleasant pictures. Coronal images at four different locations in the occipital cortex were acquired during each of eight 12-s picture presentation periods (on) and 12-s interpicture interval (off). The extent of functional activation was larger in the right than the left hemisphere and larger in the occipital than in the occipitoparietal regions during processing of all picture contents compared with the interpicture intervals. More importantly, functional activity was significantly greater in all sampled brain regions when processing emotional (pleasant or unpleasant) pictures than when processing neutral stimuli. In Experiment 2, a hypothesis that these differences were an artifact of differential eye movements was ruled out. Whereas both emotional and neutral pictures produced activity centered on the calcarine fissure (Area 17), only emotional pictures also produced sizable clusters bilaterally in the occipital gyrus, in the right fusiform gyrus, and in the right inferior and superior parietal lobules.