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Journal ofNeurology, Neurosurgery, and Psychiatry 1989;52:613-
Auditory neglect
E DE RENZI, M GENTILINI, C BARBIERI
From the Neurological Department, Modena University, Modena, Italy
SUMMARY Auditory neglect was investigated in (^) normal controls and in patients with a recent unilateral hemispheric lesion, by requiring them (^) to detect the interruptions that occurred in one ear in a sound delivered through earphones either mono-aurally or binaurally. Control patients accurately detected interruptions. One left brain damaged (LBD) (^) patient missed only once in the ipsilateral ear while seven of the 30 right brain damaged (RBD) patients missed more than one (^) signal in the mono- aural test and nine patients did the same in the binaural (^) test. Omissions were always more marked in the left ear and in the binaural test with a significant ear by test (^) interaction. The lesion ofthese patients
was in the parietal lobe (five patients) and the thalamus (four patients). The relation of auditory
neglect to auditory extinction was investigated and found to be equivocal, in that (^) there were seven
RBD patients who showed extinction, but not neglect and, more importantly, two patients who
exhibited the opposite pattern, thus challenging the view that extinction is a minor form of neglect.
Also visual and auditory neglect were not consistently correlated, the former being present in nine
RBD patients without auditory neglect and the latter in two RBD patients without visual neglect. The finding that in some RBD patients with auditory neglect omissions also occurred, though with less frequency, in the right ear, points to a right hemisphere participation in the deployment of attention not only to the contralateral, but also to the ipsilateral space.
Neglect phenomena following right brain damage
have been extensively investigated in the visual
modality, where they manifest themselves as failure to
orient attention to left-sided stimuli, which may go
undetected under conditions that should urge the
patient to survey the whole space (for example, when
required to read a sentence, which lacks (^) meaning if
only the words lying to the right are taken into
account). While visual neglect is readily apparent on a
series of tasks requiring the scanning of the environ-
ment, no convincing evidence of failure to respond to
auditory stimuli having their source located in the left
space has so far been provided. Right brain damaged
patients do show errors of localisation and lateralisa-
tion of auditory stimuli, shifting them towards the
right side'2 and sometimes answer a question ad-
dressed from the left turning their head and eyes to the
right,3 but they have never been reported to ignore a
stimulus located in^ the left space, except in response to double simultaneous stimulation. (^) Extinction, that (^) is,
the failure to perceive a stimulus in the contralateral
Address for reprint requests: Dr Ennio De Renzi, Clinica Neurologica, Via Del Pozzo 71, 1-41100 Modena, Italy.
Received 10 May 1988 and in revised (^) form 3 December 1988. Accepted 12 December 1988
ear when it is simultaneously delivered to the
ipsilateral ear, has been observed in nearly 50% of
unilaterally brain damaged patients in the early stage
of a stroke,4 but, contrary to what happens with visual
neglect, no significant association of the deficit with
right hemisphere lesions has been observed. This lack
of asymmetry in auditory extinction, which has been
confirmed in a recent investigation,5 casts some doubt
on the close relation of extinction to neglect.
Moreover, there^ were^ patients with^ long lasting extinc-
tion,4 whose injury was so located as to interrupt the
central auditory pathways in their course from the
medial geniculate body to the temporal cortex, thus
making extinction more likely to be contingent on a
sensory than an attentional impairment.
The difficulty of showing neglect in^ the auditory
modality is^ probably due^ to^ the^ physical characteris-
tics of acoustic stimuli and the (^) arrangement of the
neural apparatus transmitting them to the cortical
centres. The sound waves emitted by a left sided
acoustic source reach both ears, though for the right
one with^ delay and decreased intensity,6 and are thence
sent to both temporal cortices, though the contra-
lateral pathway is stronger. It follows that, when the
right hemisphere is damaged, the left hemisphere
remains able to perceive and attend to^ a^ sound^ coming
from the left side, due to its connections with both
ears, and can also lateralise it, though not accurately, by computing the time lag and the intensity difference with (^) which the right ear has been stimulated. It would appear that a prerequisite for bringing out auditory neglect, if it indeed (^) exists, is to confine the (^) acoustic stimulation to the ear contralateral to lesion. In this study we assessed the ability of brain- damaged patients with a recent (^) hemispheric disease (^) to monitor the interruptions that occurred at random intervals in one ear in a continuous sound delivered either unilaterally or bilaterally through earphones. We contrasted omissions in the ear contralateral and ipsilateral to the side of lesion and related them to the patients' manifestations of auditory extinction and visual neglect.
Material and methods
Subjects Fifty five patients participated in this investigation. Ten (^) were control (C) patients, hospitalised for diseases not (^) involving the brain (mean age: 56 4 yr), 15 were left (^) brain-damaged (LBD) patients (mean age: 61-2 yr) and 30 right brain- damaged (RBD) patients (mean age: 63-9 yr). Seven of the 15 LBD (^) patients were aphasic. The side of the lesion was based on clinical evidence and confirmed by CT in all patients, except two RBD patients who had negative CT findings, though showing unequivocal signs (left hemiparesis and hemianopia, respectively) of right hemisphere damage. In four RBD (^) patients CT also showed an old left vascular lesion that had been (^) clinically silent and in a fifth patient two silent left hemisphere (^) metastases in addition to a clinically evident metastasis of the right (^) hemisphere. Since neglect was the main subject of this investigation, the RBD (^) group selection was biased towards patients who presented clinically with signs of lateralised attentional disorders. Thus the (^) frequency with which neglect appears in the present sample cannot be generalised to the RBD population. Table 1 shows the clinical characteristics ofbrain-damaged patients.
Tests Patients were first submitted to pure tone audiometry to (^) rule out the presence ofmajor peripheral (^) deficits ofhearing and to ascertain whether there was an asymmetry between the (^) ear curves. If there was asymmetry the intensity of the (^) test signal delivered to the impaired ear was increased so as to equate the two (^) curves. It must be added that no patient with auditory neglect (see (^) below) showed a difference in threshold between ears.
De Renzi, Gentilini, Barbieri
Auditory attention test A sound generator delivered through (^) headphones to the patient a continuous 3000 Hz (^) pure tone at a level of 102 dB SPL; the sound lasted 4 minutes and was interrupted for 300 ms at intervals ranging from 8 to 20 ms. There were 24 interruptions, 12 per ear, to which the patient had to (^) respond by pressing the space bar ofa computer keyboard. The sound intensity could be adjusted independently in each channel in order to (^) compensate for hearing deficits, so that a (^) subjec- tively identical signal was provided to both ears in any case. The sound (^) generator was linked to an Apple II E computer by a^ versatile^ interface adaptor (6522). A computer program controlled the interruption pattern, specifically the 300 ms duration, the intervals between interruptions and the side of interruption in the binaural test. (^) Signal decay at interruption was (^) very fast, about 3 ms. The test (^) was presented in two versions, one^ mono-aural and^ the other binaural. In the mono-aural test the sound was first sent (^) to one ear until the 12 interruptions had occurred and then to the other ear, so that the patient knew where he had to focus attention. The order of ear presentation was pseudo-random. In the binaural test both ears received the sound, but the interruptions occurred quasi-randomly to either ear, with the restriction of no more than three consecutive interruptions to the same ear. In this case, therefore, the patient had to attend to both ears in order to perceive when the sound was interrupted. The following day the entire session was repeated and thus patients received (^48) signals per test, 24 in the right ear and 24 in the left ear. In the first session, patients were first familiarised with the procedure by the administration of a short version of either test with five 300 ms interruptions.
Auditory extinction Stimuli were delivered with two sound generators (75 dB), kept manually at a distance ofapproximately 10 cm from the ears, and (^) activated by pushing a button. Ten bilateral stimuli were administered, intermingled with 20 unilateral stimuli, 10 to the right and (^10) to the left ear. Responses were given by pointing with the forefinger to the ear (^) stimulated.
Visual neglect Two tests were given: (1) Reading test: The patient was (^) presented with a cardboard sheet, 41 cm x 29-5 cm, where the (^) sentence "La pera e caduta sotto l'albero" ("The pear has (^) fallen under the tree"), was written in 15 mm high (^) Letraset letters on a single line, 39 cm long. The patient was requested to read it aloud. Aphasics were encouraged to attempt reading, not (^) worrying about the errors they might make. If reading (^) proved to be impossible, they were requested to point to each word of (^) the sentence.
Table 1 Clinical characteristics ofbrain-damagedpatients
Aetiology Length ofillness* Parietalt Vascular Neoplastic (^) < 30 days > 30 days Visual neglect Aphasia involvement
RBD (^) patients (No: 30) 22 8 16 6 16 - (^15) LBD patients (^) (No: 15) 11 4 6 3 - (^7 )
*Vascular patients only. tBased on CT scan evidence.
Table 3 Clinical and (^) CTfindings in RBD patients with auditory neglect
De (^) Renzi, Gentilini, Barbieri
Pt. No. Aetiology V. Ext. T.Ext A. Ext (^) Visual neglect Locus oflesion
3 V nt nt 10/10 (^) severe R. inferior parietal infarct 4 V 10/10 nt 10/10 mild (^) R. thalamic-capsular haematoma 12 V 0/10 0/10 0/10 absent (^) R. inferior parietal + L. inferior parietal (old) infarct 15 V nt nt 4/10 severe (^) R. parietal haematoma + L. fronto-parietal (old) infarct 16 V (^) 10/10 10/10 2/10 severe (^) R. inferior parietal infarct 22 V nt 4/10 4/10 (^) severe R. thalamic-capsular infarct 23 V nt nt 9/10 severe (^) R. thalamic-capsular haematoma 28 N 10/10 10/10 0/10 absent (^) R. parietal + (^) L. parieto-occipital + L. occipital metastasis 30 V nt nt 10/10 severe (^) R. occipital and thalamic infarct
nt = not testable, because of severe somato- sensory or visual field defect. V. Ext.: visual extinction; T. Ext.: tactile extinction; A. Ext.: auditory extinction.
Discussion
The outcome of the present study provides clear
evidence that in RBD patients contralateral neglect
(that is, failure to detect a stimulus coming from the
left ear) extends to the auditory modality, provided
care is taken to confine the signal to one ear. Although
the phenomenon is already apparent in an attenuated
form when the patient focuses on the left ear, its
intensity is greatly enhanced in conditions of diffuse
attention, when the side of interruption is not known
in advance and the patient has to attend to the sound
of both ears. In this condition two RBD patients (No
23 and 30) missed practically all left ear stimuli and
two others (No 5 and 28) more than half. In three of
them (No 15, 23 and 30) omissions were still very
marked 2 to 3 months after the stroke. The length of
the testing session and the relatively rare occurrence of
interruptions have probably been instrumental in
favouring lapses in sustained attention, but the
prevalence of left ear omissions points to a specific,
lateralised deficit, which in the present series was
associated with damage to the right parietal lobe or
right thalamus, two structures known to play a pivotal
role in the circuit of lateralised attention.
It is noteworthy, however, that auditory neglect was
consistently associated neither with auditory extinc-
tion, nor with visual neglect. The finding of two
patients who had neglect, but not extinction disputes
the widely held view that extinction is but a minor
form of neglect. Taken in conjunction with compar-
able data found in the visual modality,5 and with the
three patients of the RBD group without neglect who
extinguished the majority of left ear stimuli, this
dissociation indicates that extinction does not neces-
sarily lie on a continuum of attentional disorders,
having neglect at its end, but may result from discrete
mechanisms and that any generalisation from extinc-
tion to neglect must be guarded.
The possibility first provided by the present
experiment to^ demonstrate the existence of auditory
neglect allowed us to compare its occurrence with that
of visual neglect and to gain information on the
organisation of^ the neural^ apparatus deploying atten-
tion to contralateral space. Though neglect has been
investigated mainly in the visual modality, current
theory78 tends to conceive of it as a multimodal
phenomenon, which affects the detection of con-
tralateral stimuli, whatever the sensory channel
through which they are conveyed. This may be so
because a lesion of the posterior parietal cortex, which
is the most frequent anatomical correlate of neglect in
humans91O tends to block the multiple unimodal (^) inputs
converging on it. Alternatively, it might be held that
this area is equipped to provide the neural template for
a superordinate surveyor of novel and significant
events occurring in contralateral space, the damage of
which results in failure to (^) attend to any type of stimuli
located therein. Such a hypothesis would imply that
neglect must necessarily involve all sensory inputs,
independently of the modality through which they are
transmitted, an assumption at variance with the
outcome of the present study, which (^) found nine RBD
patients with visual but not auditory neglect and two
RBD patients with auditory but not visual neglect.
These instances of dissociation are more compatible
with a (^) model envisaging a plurality of autonomous attentional control (^) systems decentralised at the level of
the single modalities, as argued by Bisiach et al " with
reference to anosognosia, and liable to produce
unimodal neglect.
So far we have focused on neglect affecting the
contralateral ear, but a failure to detect interruptions
was also apparent (^) in the ipsilateral ear of five RBD
patients, though never with the same severity as in the
contralateral ear. This finding cannot be disregarded
as an unspecific consequence of brain damage, since it
never occurred in LBD patients or in the RBD patients
without contralateral auditory neglect, even those who showed visual neglect. In two of the five patients there
was CT evidence of a previous clinically silent infarct
ofthe left hemisphere. Although a recent and clinically
manifest left brain lesion never (^) produces contralateral
neglect when occurring in isolation, the question may
Auditory neglect
be raised ofwhether an old lesion may^ play^ an^ additive effect when occurring in combination with^ a^ recent right-sided damage. On this account one would expect ipsilateral omissions to be more frequent following bilateral than unilateral (right) brain-damage, but table 2 shows that this was not the case. It is, therefore, legitimate to assume that in these^ patients,^ not^ differ- ing from patients with disease confined^ to^ the^ right hemisphere, right^ neglect^ depended^ on^ right brain damage and reflected the unique property^ of^ this hemisphere to also exert^ attentional control^ on^ the ipsilateral space. This^ hypothesis^ was^ advanced78^ to account for the much^ more^ frequent^ occurrence^ of neglect after right than^ left^ brain^ damage^ and^ found some support in^ normal studies,^ where^ EEG'2 and regional cerebral glucose metabolism data'3 suggested a right hemisphere participation^ in the^ processing^ of stimuli presented to the right space. There is also some pathological evidence^ pointing^ in^ the^ same^ direction. RBD patients have been found by Weintraub and Mesulam'4 to manifest, in addition to the classical left neglect syndrome, signs of inattention for the right space, where they missed some targets in a visual cancellation test. The interpretation of this finding is confounded by the fact that rightwards scanning unavoidably brings part of right-sided stimuli in the patient's left visual field. However, it receives some support by a study'5 showing that when single stimuli were flashed in different positions of the right visual field, those located to the left were responded to more slowly by right parietal patients. Weintraub and Mesulam's RBD patients were also found to be mildly, but significantly slower than controls on a^ tactile searching task when the target was in the^ right^ space, while no impairment in the left space was^ shown^ by LBD patients. This finding hints at a delayed^ attention in the tactical exploration of the^ ipsilateral space,^ but does not demonstrate a true neglect, comparable to that found in the contralateral space.'6 The^ right^ ear omissions, found in^ the present study, provide definite evidence for a substantial right hemisphere^ contribu- tion to the monitoring of^ right-located^ events,^ because the absence of exploratory movements in the auditory task avoids the discrepancy between body-centred space and^ eye-centred^ space^ entailed^ by^ visual^ tasks. What is surprising is that while left brain damage is apparently compensated by a well-functioning right hemisphere, the opposite is not always true.^ Is^ this asymmetry to be taken as^ evidence that^ right^ space surveillance is exerted more powerfully by the ipsilateral right hemisphere than the contralateral left hemisphere? More data are needed, particularly on^ the behaviour of LBD patients, before a^ conclusion^ can^ be reached. The auditory attention^ test^ appears^ to provide a good paradigm for^ pursuing^ this^ line^ of research.
We thank Dr^ C^ A^ Porro^ for his^ assistance^ in the
preparation of^ the computer^ program.^ Dr P^ Faglioni
for statistical advice and^ the Centro^ di^ Calcolo
dell'Universita di Modena^ for^ having provided^ its
facilities. This research was^ supported by^ a^ CNR grant and an MPI^ grant^ to^ Dr^ E^ De^ Renzi.
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