52252ournal ofNeurology, Neurosurgery, and Psychiatry 1997;62:522-526 J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.62.5.522 on 1 May 1997. Downloaded from SHORT REPORT Sound movement detection deficit due to a brainstem lesion T D Griffiths, D Bates, A Rees, C Witton, A Gholkar, G G R Green Abstract lesion involving the trapezoid body, suggesting Auditory psychophysical testing was car- that convergence at the level of the superior ried out on a patient with a central pon- olive is needed for human sound movement tine lesion involving the trapezoid body, analysis. who presented with a deficit in sound localisation and sound movement detec- tion. A deficit in the analysis of time and Methods intensity differences between the ears was CASE REPORT found, which would explain the deficit in The patient presented at the age of 45 with detection of sound movement. The recent hearing symptoms. She described diffi- impaired detection of sound movement, culty with making out some speech sounds, due to a lesion interfering with conver- particularly in crowded rooms, and a difficulty gence of auditory information at the with sound localisation such that she had superior olive, suggests this structure to become unable to detect which of three well be critical for human sound movement separated telephones in her office was ringing. analysis. The patient also had difficulty with the per- ception of moving sounds. For example, she (7 Neurol Neurosurg Psychiatry 1997;62:522-526) was unable to detect which way a train was travelling when she was standing on a plat- Department of form, on the basis of sound alone. She had a Physiological Sciences, Keywords: sound; sound movement; brainstem; history of more than 10 years of right sided Newcastle University human; lesion headaches and more recent right sided tinni- Medical School, Newcastle upon Tyne, tus, in addition to episodes of rotatory vertigo. The analysis of movement in the sys- NE2 4HH, UK auditory Neurological examination was remarkable http://jnnp.bmj.com/ T D Griffiths tem requires changes in the phase and ampli- only for the presence of nystagmus on right A Rees C Witton tude of the sounds arriving at the two ears to lateral gaze. G G R Green be compared. Both processes depend on the Brain MRI with gadolinium showed an Department of Clinical convergence of information from the ears. enhancing lesion in the central pons (fig 2), Neuroscience, This convergence first occurs at the superior between the dorsal pontine tegmentum and Newcastle University olive, where the input from the ipsilateral ventral pons and extending rostrally, but not Medical School, cochlear nucleus converges Newcastle upon Tyne, with that from the as far as the midbrain. Angiography of the pos- NE2 4HH, UK contralateral cochlear nucleus, relayed via the terior circulation was normal; the lesion was on September 28, 2021 by guest. Protected copyright. T D Griffiths trapezoid body (fig 1). Convergence also thought to be a capillary vascular malforma- D Bates occurs higher in the pathway at the level of the tion. Welicome Department colliculi. Neurophysiological studies in ani- of Cognitive Neurology, Institute of mals have shown that the cells in the medial PSYCHOPHYSICAL TESTING Neurology, 12 Queen superior olive (MSO) respond to timing or Auditory testing was carried out with com- Square, London, phase differences between the ears in a linear puter generated stimuli presented over head- WC1N 3BG, UK T D Griffiths fashion,1 2 whereas cells at the level of the infe- phones in a sound proofed room. The tests Neuroradiology rior colliculus show non-linearities consistent with modulated sounds used a two alternative Department, with a selective response to sound movement.3 forced choice procedure, with a pure tone ref- Newcastle General Selective responses to sound movement have erence interval with at least 10 trials per point Hospital, Westgate Rd, also been shown in animals in the superior col- and at least five stimulus levels. Newcastle upon Tyne, NE4 6BE, UK liculus,4 primary auditory cortex,5 6 7 and in A Gholkar humans in the multimodal cortex.8 Lesions Correspondence to: producing deficits in the detection of sound Results Dr T D Griffiths, Department of Physiological movement have not previously been reported PSYCHOPHYSICAL ASSESSMENT Sciences, Newcastle in humans, although we have recently Pure tone and fixed interaural phase difference University Medical School, a a Newcastle upon Tyne, reported patient with right hemispheric detection NE2 4HH,UK. stroke and a deficit in the detection of phase Pure tone thresholds disclosed a low frequency Received 11 June 1996 and amplitude changes simulating motion.9 sensorineural hearing loss of 35 dB on the left and in final revised form 21 January 1997 We report here a patient with a deficit in and 25 dB on the right at 500 Hz (fig 3). Accepted 23 January 1997 sound movement analysis due to a brainstem These losses were corrected for in the other Sound movement detection deficit due to a brainstem lesion 523 J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.62.5.522 on 1 May 1997. Downloaded from Cortex L R MGN SC A -. IC IC A Lateral lemniscus DCN DCN A A A LSO MSO MSO LSO MNTB MNTB A. VCN A A .......-- ... i i A -A.VCN A Cochlea Cochlea Trapezoid body Figure 1 Simplified diagram of the auditory pathway showing the convergence of the inputfrom both ears at the right sided brainstem auditory nucleii. This is based primarily on pathways describedfor the cat and other mammals'4 although anatomical differences between species (including humans) are described'5 16 (J K Moore, personal communication). In particular, there is debate about the relative importance of the pathway via the medial nucleus of the trapezoid body (MNTB) and lateral superior olive (LSO) in humans. All connections would be reflected in the midline. The medial superior olive (MSO) is shown to be the first point at which binaural convergence occurs via the trapezoid body. Convergence also occurs at higher levels, including the level ofthe nucleus of the lateral lemniscus (not shown) and inferior colliculus (IC). The diagram shows a ventral pathway, via the ventral cochlear nucleus (VCN), trapezoid body, and MSO, thought to be important in animals for the analysis ofspatial information. A dorsal pathway, via the dorsal cochlear nucleus (DCN) and IC, is also shown, which is involved in animals in the analysis ofcomplex waveforms. MGB = medial geniculate body, SC = superior colliculus. psychophysical tests by using sensation levels mean of 180 for untrained controls. A further http://jnnp.bmj.com/ to match the stimulus at each ear, and addi- test was carried out to check whether the tionally checking that the binaurally presented patient was using phase differences between 500 Hz tones used in the other tests produced the ears, or was simply detecting the frequency a midline sound image. The threshold for modulation produced by the phase changes detection of a fixed phase difference between considered at either ear alone. This was done the ears at 500 Hz was 2.250 for a sound by playing the same phase modulated sound which seemed to move to the right and 3.450 into the right or the left ear without a tone in on September 28, 2021 by guest. Protected copyright. for a sound which seemed to move to the left, the opposite ear for comparison. The patient which are within normal limits.'0 However, the performed at chance level on either side up to a patient found the task difficult and needed modulation depth of 1000, in the same way as repeated trials to achieve these normal values. normal listeners, confirming that she was using phase differences between the ears to Interaural phase modulation detection (sinusoidal detect the IPM stimulus. and ramp) Further testing was carried out with another Detection of changes in the phase or timing 500 Hz stimulus which contained a phase between the ears is used at low frequency to ramp, such that the phase advanced in one ear detect sound movement. Figure 4 shows the as it was delayed in the other ear. This stimulus psychophysical function for detection of a contains identical phase changes to a sound sound in which the phase is constantly moving in an arc around the head in one direc- changed between the ears: sinusoidal interau- tion, and was used as a more "physiological" ral phase modulation (IPM). The stimulus is stimulus than one moving from side to side, in perceived as a sound which moves from side to which repetition of apparent sound source side by normal observers, and was used as a positions could provide an extra cue. The more exacting test of the analysis of differ- patient was unable to perceive sound move- ences in phase between the ears. The patient ment during presentation of such a ramp over was able to perceive this stimulus as sound 300 ms or 500 ms in either direction, even movement, and had a detection threshold of when the magnitude of the phase change was 240 (by Weibull analysis) compared with a equivalent to 1800 . Figure 5 shows the perfor- 524 Griffiths, Bates, Rees, Witton, Gholkar, Green Figure 2 Tl weighted gadolinium enhanced J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.62.5.522 on 1 May 1997. Downloaded from MRI. (A) Transverse section at level ofthe midpons showing the central location of the lesion. (B) Midsagittal section showing lesion to extend rostrally to a point below the midbrain. cJ L-,aL) o O (-) 20 O0 0 10 20 30 40 50 Modulation depth (0) Figure 4 Psychophysicalfunction showing detection of interaural phase modulation (IPM) as a function of modulation depth expressed as degrees.