Alan R. Palmer

''Sparse'' Temporal Sampling in Auditory fMRI

The use of functional magnetic resonance imaging (fMRI) to explore central auditory function may be compromised by the intense bursts of stray acoustic noise produced by the scanner whenever the magnetic resonance signal is read out. We present results evaluating the use of one method to reduce the effect of the scanner noise: “sparse” temporal sampling. Using this technique, single volumes of brain images are acquired at the end of stimulus and baseline conditions. To optimize detection of the activation, images are taken near to the maxima and minima of the hemodynamic response during the experimental cycle. Thus, the effective auditory stimulus for the activation is not masked by the scanner noise.

A neural code for low-frequency sound localization in mammals.

We report a systematic relationship between sound-frequency tuning and sensitivity to interaural time delays for neurons in the midbrain nucleus of the inferior colliculus; neurons with relatively low best frequencies (BFs) showed response peaks at long delays, whereas neurons with relatively high BFs showed response peaks at short delays. The consequence of this relationship is that the steepest region of the function relating discharge rate to interaural time delay (ITD) fell close to midline for all neurons irrespective of BF. These data provide support for a processing of the output of coincidence detectors subserving low-frequency sound localization in which the location of a sound source is determined by the activity in two broad, hemispheric spatial channels, rather than numerous channels tuned to discrete spatial positions.

Neuronal responses to amplitude‐modulated and pure‐tone stimuli in the guinea pig inferior colliculus, and their modification by broadband noise

Neuronal responses were recorded to pure and to sinusoidally amplitude-modulated (AM) tones at the characteristic frequency (CF) in the central nucleus of the inferior colliculus of anesthetized guinea pigs. Temporal (synchronized) and mean-rate measures were derived from period histograms locked to the stimulus modulation waveform to characterize the modulation response. For stimuli presented in quiet, the modulation gain at low frequencies of modulation (approx less than 50 Hz) was inversely proportional to the neurons mean firing rate in response to both the modulated stimulus and to a pure tone at an equivalent level. In 43% of units the mean discharge rates in response to the AM stimuli were greatest for those modulation frequencies that generated the largest temporal responses. These discharge-rate maxima occurred at signal intensities corresponding to the steeply sloping part of the neurons pure-tone rate-intensity function (RIF). The change in mean-rate response to modulated stimuli, as a function of intensity, was qualitatively similar to the pure-tone RIF. Adding broadband noise to the modulated stimulus increased the neurons temporal response to low modulation frequencies. This increase in modulation gain was correlated with mean firing rate in response to the modulation but did not bear a simple relationship to the noise-induced shift in the RIF measured for a pure tone.

Identification and localisation of auditory areas in guinea pig cortex

Abstract. The organisation of guinea pig auditory cortex was studied by combining histological methods with microelectrode mapping. This allowed the location of seven auditory areas to be determined in relation to the visual and primary somatosensory areas. The auditory areas were identified by single-unit recordings and their borders defined by evoked potential mapping. The visual areas were identified by their relatively high densities of myelinated fibres, while the primary somatosensory cortex was identified by its characteristic barrels of high cytochrome oxidase (CYO) activity in layer IV. The auditory region had moderate levels of CYO and myelin staining. When staining was optimal, there was a clear edge to the moderate CYO activity, which apparently corresponds to the dorsal border of the primary auditory area (AI) and the other core field that lies dorsocaudal to it (DC). Thus the primary somatosensory area and the visual and auditory regions were separated from each other by a region with lower levels of CYO and myelin staining. The ventral borders of AI and DC could not be determined histologically as there were no sharp transitions in the levels of CYO or myelin staining. The two core areas were partially surrounded by belt areas. The dorsorostral belt and most of the belt around DC responded more strongly to broad-band stimuli than pure tones, while the ventrorostral belt, small field and a belt zone ventral to the rostral part of DC responded better to pure tones. Units in the small field (S) typically had higher thresholds and broader tuning to pure tones than AI, while units in the ventrorostral belt typically had longer onset latencies and gave more sustained responses than units in AI.

Modulation and task effects in auditory processing measured using fMRI

Active listening has been reported to elicit a different sensory response from passive listening and is generally observed as an increase in the magnitude of activation. Sensory activation differences may therefore be masked by the effect of attention. The present study measured activation induced by static and modulated tones, while controlling attention by using target‐discrimination and passive listening tasks. The factorial design enabled us to determine whether the stimulus‐induced activation in auditory cortex was independent of the information‐processing demands of the task. Contrasted against a silent baseline, listening to the tones induced widespread activation in the temporal cortex, including Heschls gyrus (HG), planum temporale, superior temporal gyrus (STG), and superior temporal sulcus. No additional auditory areas were recruited in the response to modulated tones compared to static tones, but there was an increase in the response in the STG, anterior to HG. Relative to passive listening, the active task increased the response in the STG, posterior to HG. The active task also recruited regions in the frontal and parietal cortex and subcortical areas. These findings indicate that preferential responses to the changing spectro‐temporal properties of the stimuli and to the target‐discrimination task involve distinct, non‐overlapping areas of the secondary auditory cortex. Thus, in the present study, differences in sensory activation were not masked by the effects of attention. Hum. Brain Mapping 10:107–119, 2000.

Time-course of the auditory BOLD response to scanner noise

It is a concern for auditory fMRI studies that acoustic noise generated by the scanner produces an auditory response that can confound stimulus‐induced activation. To establish how to minimize this problem, the present study mapped the time‐course of the auditory response to a burst of acoustic scanner noise by employing a single‐event method. Recorded bursts of scanner noise were interspersed with clustered‐volume acquisitions at a range of stimulus‐to‐imaging delays to map the response with a temporal resolution of 1 sec. There were strong responses (1.5% signal change) to scanner noise in primary and secondary auditory cortex. In both cortical areas, the mean response rose to a peak by 4–5 sec after stimulus onset and decayed after a further 5–8 sec. The time course indicates that noise contamination in auditory fMRI can be substantially reduced by using a 9–12‐sec repetition time, thus maximizing the dynamic range available for displaying the response to acoustical stimuli of interest. Magn Reson Med 43:601–606, 2000.

Sound-Level Measurements and Calculations of Safe Noise Dosage During EPI at 3 T

This paper describes systematic methods for measuring and controlling sound levels within a magnetic resonance scanner. The methods are illustrated by application to the acoustic noise generated by a 3 T scanner during echoplanar imaging (EPI). Across five measurement sessions, sound pressure levels at the center of the head gradient coil ranged from 122 to 131 dB SPL [123 to 132 dB(A)]. For protection against damaging noise exposure, UK and US industrial guidelines stipulate that the maximum permitted daily noise dosage is equivalent to 90 dB(A) for 8 hours, where noise dosage is a function of the level of an acoustic signal and the length of exposure to it. Without hearing protection, this equivalent level would be exceeded by less than 5 seconds of exposure to the measured levels of scanner acoustic noise. These findings highlight the importance of noise reduction and hearing protection for those exposed to the acoustic noise generated during EPI. J. Magn. Reson. Imaging 2000;12:157–163.

Interaural delay sensitivity and the classification of low best-frequency binaural responses in the inferior colliculus of the guinea pig

Monaural and binaural response properties of single units in the inferior colliculus (IC) of the guinea pig were investigated. Neurones were classified according to the effect of monaural stimulation of either ear alone and the effect of binaural stimulation. The majority (309/334) of IC units were excited (E) by stimulation of the contralateral ear, of which 41% (127/309) were also excited by monaural ipsilateral stimulation (EE), and the remainder (182/309) were unresponsive to monaural ipsilateral stimulation (EO). For units with best frequencies (BF) up to 3 kHz, similar proportions of EE and EO units were observed. Above 3 kHz, however, significantly more EO than EE units were observed. Units were also classified as either facilitated (F), suppressed (S), or unaffected (O) by binaural stimulation. More EO than EE units were suppressed or unaffected by binaural stimulation, and more EE than EO units were facilitated. There were more EO/S units above 1.5 kHz than below. Binaural beats were used to examine the interaural delay sensitivity of low-BF (BF < 1.5 kHz) units. The distributions of preferred interaural phases and, by extension, interaural delays, resembled those seen in other species, and those obtained using static interaural delays in the IC of the guinea pig. Units with best phase (BP) angles closer to zero generally showed binaural facilitation, whilst those with larger BPs generally showed binaural suppression. The classification of units based upon binaural stimulation with BF tones was consistent with their interaural-delay sensitivity. Characteristic delays (CD) were examined for 96 low-BF units. A clear relationship between BF and CD was observed. CDs of units with very low BFs (< 200 Hz) were long and positive, becoming progressively shorter as BF increased until, for units with BFs between 400 and 800 Hz, the majority of CDs were negative. Above 800 Hz, both positive and negative CDs were observed. A relationship between CD and characteristic phase (CP) was also observed, with CPs increasing in value as CDs became more negative. These results demonstrate that binaural processing in the guinea pig at low frequencies is similar to that reported in all other species studied. However, the dependence of CD on BF would suggest that the delay line system that sets up the interaural-delay sensitivity in the lower brainstem varies across frequency as well as within each frequency band.

Descending Projections From Auditory Cortex Modulate Sensitivity in the Midbrain to Cues for Spatial Position

The function of the profuse descending innervation from the auditory cortex is largely unknown; however, recent studies have demonstrated that focal stimulation of auditory cortex effects frequency tuning curves, duration tuning, and other auditory parameters in the inferior colliculus. Here we demonstrate that, in an anesthetized guinea pig, nonfocal deactivation of the auditory cortex alters the sensitivity of populations of neurons in the inferior colliculus (IC) to one of the major cues for the localization of sound in space, interaural level differences (ILDs). Primary and secondary auditory cortical areas were inactivated by cooling. The ILD functions of 46% of IC cells changed when the cortex was inactivated. In extreme cases, the ILD functions changed from monotonic to nonmonotonic during cooling and vice versa. Eight percent of the cells became unresponsive after deactivation of the auditory cortex. Deactivation of the cortex has previously been shown to alter the maximum spike count of cells in the IC; the change in normalized ILD functions is shown to be separate from this effect. In some cases, the ILD function changed shape when there was no change in the maximum spike count and in other cases there was no change in the shape of the ILD function even though there was a large change in the maximum spike count. Overall, the sensitivity of the IC neural population to ILD is radically altered by the corticofugal pathway.

The ability of inferior colliculus neurons to signal differences in interaural delay

Sound localization in humans depends largely on interaural time delay (ITD). The ability to discriminate differences in ITD is highly accurate. ITD discrimination (Δ ITD) thresholds, under some circumstances, are as low as 10–20 μs. It has been assumed that thresholds this low could only be obtained if the outputs from many neurons were combined. Here we use Receiver Operating Characteristic analysis to compute neuronal Δ ITD thresholds from 53 cells in the inferior colliculus in guinea pigs. The Δ ITD thresholds of single neurons range from several hundreds of μs down to 20–30 μs. The lowest single-cell thresholds are comparable to human thresholds determined with similar stimuli. This finding suggests that the highly accurate sound localization of human observers is consistent with the resolution of single cells and need not reflect the combined activity of many neurons.