Historical Considerations

Following Wernicke's (1874) seminal description of “sensory aphasia,” Kussmaul (1877) noted similar deficits in auditory comprehension in a patient who did not demonstrate the coexisting problems with reading or the copious “paraphasias” (a term he coined) that Wernicke had noted. Kussmaul postulated that this symptom complex constituted a distinguishable syndrome “word deafness” that resulted from destruction of the first left temporal gyrus. He contrasted this with an analogous disturbance in processing language in the visual modality, “word blindness,” which he believed was secondary to left angular gyrus and supramarginal gyrus lesions. When the two syndromes occurred together, he suggested, they represented Wernicke's sensory aphasia.

Lichtheim (1885) also regarded “isolated word deafness” as a distinct clinical entity, characterizing it in terms of selective deficits in auditory language comprehension, repetition, and writing to dictation. He supported this with a description of a case who demonstrated early symptoms of Wernicke's aphasia that improved rapidly, leaving a more selective pattern of deficits that spared volitional speech, reading, copying written material, and spontaneous writing (p. 460). While Kussmaul had implicated destruction of auditory cortex, Lichtheim speculated that word deafness resulted from a deep left temporal lesion that essentially isolated Wernicke's area from the “auditory reception center” (primary auditory cortex). His conceptualization implied that Wernicke's area and auditory cortex might independently be capable of normal or near normal functioning. Subsequently, several case studies confirmed an association of PWD with deep unilateral superior temporal lesions (Liepmann & Storch, 1902; Schuster & Taterka, 1926).

A number of reports also emerged suggesting that PWD could result from bilateral temporal lesions (Pick, 1892; Déjerine & Serieux, 1898; Ballet, 1903; Barrett, 1910; Henschen, 1919, 1920). In contrast to the unilateral cases, these patients frequently demonstrated persisting aphasic disturbances or collateral symptomatology suggestive of a resolving general auditory agnosia or cortical deafness (Buchman et al., 1986). The rarity of cases fully meeting criteria for PWD prompted some to question the existence of the syndrome. Pierre Marie (1906) remarked in no uncertain terms that PWD was “a simple myth” stating “I must declare, first of all, that to my knowledge pure word deafness does not exist from either the clinical or the anatomical pathological point of view … it is impossible to find an authentic case of this pretended clinical form” (translated by Cole & Cole, 1971, pp. 77–78). Head (1926) concurred, noting that in every instance where case reports provided sufficient detail, nonverbal perceptual impairment existed or there was clear evidence of an aphasic disturbance apparent in problems executing both written and oral commands. Despite persisting concerns over definitional issues, many cases labeled as PWD were subsequently reported with unilateral left temporal or bitemporal lesions, which did not entirely comply with the original criteria.

The broadening concept of PWD arguably contributed to confusion regarding its validity, its basis, and its boundaries that continues to the present day. Both the selectivity for verbal material and the preservation of other language functions remain focal points in contemporary controversies (Goldstein, 1974; Buchman et al., 1986). A current review of the literature reveals a predominance of cases (∼72%) secondary to bitemporal infarcts, typically involving fairly symmetric cortico-subcortical lesions compromising middle and posterior regions of the superior temporal gyrus (Poeppel, 2001), some with sparing of Heschl's gyrus (Bauer & Zawacki, 2000). Word deafness resulting from unilateral lesions is more rarely reported, and in only a few cases has the location of the lesion been adequately delineated (Hamanaka et al., 1980; Kamei et al., 1981; Metz-Lutz & Dahl, 1984; Takahashi et al., 1992; Wang et al., 2000). In all but one unilateral case, PWD has been reported in association with left hemisphere pathology.

As a consequence of both the higher proportion of bitemporal lesions and the general rarity of cases that adhere to strict diagnostic criteria, prevalent views regarding the functional basis of PWD are disproportionately influenced by studies in which word deafness was identified as a symptom mixed with other aphasic components (Miceli, 1982; Buchman et al., 1986; Buchtel & Stewart, 1989; Praamstra et al., 1991) or with features of a broader auditory recognition disorder (Auerbach et al., 1982; Vignolo, 1982). As a case in point, the only report of PWD resulting from a unilateral right temporal lesion (Roberts et al., 1987) is a patient who lost his ability to recognize both spoken words and musical tunes and arguably should not be regarded as a “pure” case of word deafness. In reviewing the literature, Buchman et al. (1986) suggested that the modifier “pure” be dropped but supported the concept that “word deafness” was a distinct clinical entity.

A Prototypical Presentation of PWD

NH represents one of the rare instances where the clinical picture conforms well to the original descriptions of PWD. Consistent with Lichtheim's description, she exhibited early signs of a broader aphasic disturbance resembling a Wernicke's aphasia that rapidly resolved in the course of a couple of weeks, leaving her with a remarkably circumscribed disturbance of auditory language comprehension. She demonstrated moderate to severe difficulties in understanding and repeating spoken language with otherwise intact speech production and nonauditory language comprehension. Both reading and spontaneous writing were preserved. In addition, there was no evidence of a broader auditory agnosia. She demonstrated intact environmental sound recognition and reported no change or difficulties in her appreciation of music, although she complained that she could no longer understand the lyrics. Her peripheral hearing sensitivity in the frequency range most critical to speech was broadly within normal limits, although her audiogram showed mildly raised thresholds at 4 and 8 kHz in the ear contralateral to her lesion.

Similar audiological findings have been described in other unilateral cases of PWD (e.g., Saffran et al., 1976) although interaural disparities in sensitivity have also been evident at somewhat lower (250–1000 Hz) frequencies (Takahashi et al., 1992; Wang et al., 2000). By comparison, patients with word deafness secondary to bitemporal lesions commonly demonstrate bilateral increases in pure-tone thresholds (Lhermitte et al., 1971; Kanshepolsky et al., 1973; Phillips & Farmer, 1990) that are also frequently associated with a gradient whereby higher frequencies (≥4 kHz) are more affected (Jerger et al., 1972; Auerbach et al., 1982; Motomura et al., 1986; Tanaka et al., 1987; Yaqub et al., 1988; Praamstra et al., 1991; Griffiths, Rees & Green, 1999).

Analysis of NH's ability to perceive speech revealed a substantial impairment in her ability to distinguish between stop consonants while her perception of vowels was significantly better. This pattern of phonemic imperception has been previously described in PWD (Saffran et al., 1976; Auerbach et al., 1982; Miceli, 1982; Yaqub et al., 1988) but is not specific to it. Inordinate difficulty with consonant processing can emerge in aphasia (Miceli et al., 1978; Baker et al., 1981; Gow & Caplan, 1996; Caramazza et al., 2000) and problems with specific stop consonants (for example, alveolars t, d) can be secondary to moderate hearing loss (Walden & Montgomery, 1975). However, NH's difficulties with phonemic perception are both more severe and pervasive than those typically associated with aphasia or mild to moderate hearing loss. In the context of her overall presentation, they suggest that a fundamental breakdown exists in processes that mediate the mapping of acoustic features of consonants onto discrete phonological representations or in the representations themselves. Viewed from the perspective of current models of speech perception (McClelland & Elman, 1986; Franklin, 1989; Marslen-Wilson & Warren, 1994; Frauenfelder & Floccia, 1998; Norris et al., 2000), this would impede the matching of acoustic input with lexical entries that in turn could result in failures to activate the retrieval of meaning attributes of words in the semantic system.

The prelexical impairment in auditory analysis associated with “word sound deafness” can be contrasted with “word meaning deafness” (Bramwell, 1927; Kohn & Friedman, 1986) in which patients have severe difficulties understanding auditory language but are able to repeat speech and write to dictation. Preservation of the ability to repeat speech in these cases suggests that their analysis of phonological information is relatively intact (but see Tyler & Moss, 1997). Rather, the disruption of language comprehension in word meaning deafness appears to occur at the level of lexical access, possibly secondary to a failure to match the intact phonological code with corresponding lexical representations or to a “post access” failure of lexical items to activate corresponding representations in the semantic system (Ellis, 1984; Kohn & Friedman, 1986; Franklin et al., 1996).

NH also exhibited significant perturbations in dichotic listening performance that are consistent with previous descriptions of unilateral cases of PWD (Albert & Bear, 1974; Saffran et al., 1976). Specifically, she demonstrated extinction of words presented to the right ear during dichotic stimulation and relative suppression of right ear recall when listening to dichotic CV syllables. A strong left ear advantage on dichotic listening tasks has also been observed in patients with aphasia and interpreted as evidence of functional neuroplasticity and a greater role of right hemisphere mechanisms in mediating speech processing (Moore & Papanicolaou, 1988, 1992). It is somewhat unusual to obtain complete or near complete extinction of the right ear in aphasia (Niccum et al., 1986), although it can occur with lesions to Heschl's gyrus or geniculotemporal pathways with or without aphasia.

Several factors may account for this pattern in NH. First, the extent and distribution of her lesion likely prevents right ear input from reaching Wernicke's area via crossed geniculocortical auditory pathways. Right ear input may conceivably reach Wernicke's area via transcallosal pathways, although it must compete against left ear input arriving at right auditory cortex via stronger contralateral pathways. Given that contralateral pathways are functionally predominant over ipsilateral channels, this competition is biased against the right ear input. Degradation of the signal may result from the circuitous path to the language dominant hemisphere, and this may be further affected by alterations in hearing competence seen contralateral to hemispheric lesions (Linebaugh, 1978; Niccum & Speaks, 1991). Finally, it is also possible that transcallosal pathways have been compromised by the subcortical extension of her lesion (Gazzaniga et al., 1973). Selective attention appeared to have little effect on this asymmetry.

It is noteworthy that NH showed generally lower overall performance on dichotic word tasks than has been noted in other unilateral cases of PWD. We used an open set of words while both Saffran et al. (1976) and Albert and Bear (1974) used small (≤12) closed sets of dichotic stimuli (monosyllabic names and digits). Because patients with PWD appear to make use of contextual cues (Saffran et al., 1976; Best & Howard, 1994), repeated presentation of distinct stimuli from a closed set may have contributed to the relatively better overall accuracy in those studies.

Word Deafness, Speech Processing, and Temporal Imperception

The fundamental nature of the processing disturbance that characterizes PWD has not been firmly established, nor is it clear that the same mechanism is operative in all cases. Recent attempts to identify the functional locus of their verbal auditory recognition disorder have focused on detailed analyses of their difficulties with speech perception (Denes & Semenza, 1975; Saffran et al., 1976; Auerbach et al., 1982; Yaqub et al., 1988; Praamstra et al., 1991). A key issue concerns the basis for the dissociation between consonant and vowel perception and whether a lawful breakdown occurs in their processing of particular phonetic features during consonant perception.

Vowels are characterized acoustically by a formant frequency structure that maintains a relatively steady state for 100–150 ms. Although not invariably the case (Tanaka et al., 1987; Praamstra et al., 1991; Tanji et al., 2003), the reasonably static cues for vowel perception, such as the frequency of the first formant (F1) and the relative spacing between F1 and F2 (Delattre et al., 1952; Ladefoged, 2001), are generally processed without substantial difficulty in PWD, even in patients with bitemporal lesions (Auerbach et al., 1982; Miceli, 1982; Yaqub et al., 1988).

By contrast, the processing of consonants is impaired in both unilateral and bitemporal cases of PWD (Denes & Semenza, 1975; Auerbach et al., 1982; Yaqub et al., 1988; Kazui et al., 1990; Godefroy et al., 1995; Jacobs & Schneider, 2003). This has been observed when tested by means of natural CV syllables (Denes & Semenza, 1975; Saffran et al., 1976) as well as computer-synthesized speech sounds (Saffran et al., 1976; Miceli, 1982). The perception of consonants necessitates successful online perceptual elaboration of short-term acoustic features in the speech signal. Cues important for the perception of stop consonants of English (p, t, k, b, d, g) include the spectrum of brief (5 and 15 ms) noise (consonantal) bursts (Fant, 1973), and the rate, duration, and direction of rapid (20–50 ms) formant frequency transitions (Delattre et al., 1952; Liberman et al., 1967; Keating & Blumstein, 1978; Diehl, 1981). The frequency of the burst and the trajectory (rising vs. falling) of formant transitions give rise to the perception of different places of articulation (labial, alveolar, or velar). There are also multiple cues to distinguish voiced (b, d, g) from voiceless (p, t, k) consonants. A primary cue related to voiced-voiceless distinctions is the “voice-onset time,” which corresponds to the time lag between the consonantal burst and the onset of voicing (the first glottal pulse).

Some studies have suggested that patients with PWD demonstrate a systematic breakdown involving the coding of particular phonetic features. This is of considerable interest because it may specify the level of phonemic processing where problems arise (Saffran et al., 1976; Caramazza et al., 1983; Metz-Lutz & Dahl, 1984). Saffran et al. (1976) noted greater difficulty in identifying consonants differentiated by voiced-voiceless distinctions than place of articulation in a patient with word deafness secondary to left hemisphere pathology. More frequently, however, the converse pattern has been observed (Miceli, 1982; Yaqub et al., 1988), or patients demonstrate roughly equal problems with consonant perception whether the critical feature contrast is dependent on place or voicing cues (Tanaka et al., 1987; Praamstra et al., 1991). Given the relatively small number of cases, variations in underlying pathology, and differences in methodology, there is insufficient information at present to discern whether systematic dissimilarities in consonant perception may exist between patients with unilateral and bilateral lesions. However, the observed patterns of error do not appear to be predictable on the basis of problems at the level of phonological representation. Consequently, it has been suggested that their difficulties with speech perception may be related to prephonemic disturbances (Saffran et al., 1976; Auerbach et al., 1982).

Prephonemic Disturbance in Word Deafness

The precise nature and extent of prephonemic disturbances associated with PWD remain to be elaborated. A number of studies have suggested that deficits in temporal resolution may be key to their difficulties in processing speech. While normal individuals demonstrate click fusion thresholds on the order of 1 to 3 ms (Miller & Taylor, 1948; Patterson & Green, 1970; Hirsh, 1975), it has been reported that patients with PWD require 15–300 ms between two clicks before they are able to reliably make this discrimination (Albert & Bear, 1974; Auerbach et al., 1982; Tanaka et al., 1987; Best & Howard, 1994; Godefroy et al., 1995). Auerbach et al. (1982) proposed that this elevated threshold reflected impaired auditory temporal acuity, which in turn could cause special difficulties with consonant perception by impeding the analysis of rapid formant frequency transitions.

The link between impairment of auditory temporal resolution and problems with specific aspects of speech perception or language comprehension in PWD has remained speculative. Indirect evidence supporting an association may be garnered from a study by Godefroy et al. (1995) who followed a patient with “auditory agnosia” in the course of his recovery. They found that click fusion thresholds assessed in the acute stage were significantly elevated. However, as the word deafness resolved, there was a corresponding normalization of click fusion thresholds. The parallel recovery of word deafness and click fusion strengthens the argument for a common underlying disturbance, although clearly it is not possible to suggest causal relations from such correlations.

The precise nature of the temporal processing deficits indexed by faulty click fusion also remains at issue. Kanshepolsky et al. (1973) found that as the duration of auditory stimuli became very short, sound intensity had to be raised appreciably (20 to 25 dB) in order for their patient with word deafness to hear the stimulus. A few studies have shown that these problems tend to co-occur in patients with word deafness secondary to bitemporal infarction, particularly with lesions involving or extending into subcortical white matter (Motomura et al., 1986; Tanaka et al., 1987). However, Buchtel and Stewart (1989) suggest that poor temporal resolution is evident in PWD in the absence of difficulties perceiving brief stimuli in isolation. Noting that their patient with PWD was completely unable to perceive clicks due to their brevity, they utilized a modified fusion task, replacing clicks with 30 ms tone bursts that their patient had no difficulty hearing. Manipulating the duration of the silent ISI between these tone bursts, they found that their patient demonstrated profound difficulties in discriminating one from two tones presented in rapid succession. Whereas normal subjects reliably differentiated two tones when separated by silent intervals of approximately 15 ms, their patient required a silent gap of approximately 250 ms.

Based on observations of a frequent co-occurrence of abnormal intensity-duration functions and elevated fusion thresholds, Tanaka et al. (1987) speculated on a common neurophysiological basis for these diverse disturbances of timing. They suggested that such problems might be explicable in terms of abnormal persistence of neural activity, prolonged refractory periods, or slow initial recruitment. Some studies have observed that timing anomalies are also evident in PWD in the perception of rapid visual events (Best & Howard, 1994; Tanaka et al., 1987) raising the possibility of a supramodal timing deficit. Extending a conceptualization by Auerbach et al. (1982), Best and Howard (1994) suggested that a slow or inconsistent neural clock may the most parsimonious explanation for the diverse temporal processing deficits associated with PWD. They conceived of this biological timing mechanism in terms of a reciprocal loop from the cortex to the cerebellum and suggested that it may serve as a central timing mechanism for several neural systems.

Temporal Processing in Unilateral Cases

A problem with the slow clock hypothesis and other accounts positing that PWD is based in fundamental disturbances of temporal resolution is that the supporting data are derived almost entirely from patients with bilateral lesions. Only one study has examined click fusion in a unilateral case of PWD, and while the findings were abnormal (Albert & Bear, 1974), the observed threshold (15 ms) was substantially lower than that described in several cases of word deafness secondary to bitemporal lesions (30 to 300 ms) (Auerbach et al., 1982; Motomura et al., 1986; Tanaka et al., 1987).

Evidence from NH suggests that temporal processing deficits can exist in PWD in the absence of basic deficiencies in resolving distinct auditory events. NH demonstrated a normal click fusion threshold, yet had profound difficulties with the spectrotemporal analysis of transient modulations in formant frequency occurring within a temporal window of up to 200 ms. Because short-term dynamic patterns such as frequency modulations (FM) are ubiquitous to speech and serve as fundamental cues to the phonemic identification of consonants, the observed deficits would pose significant obstacles in understanding spoken language. By contrast, she appeared able to process slower modulations. Although not specifically examined, this may support satisfactory processing of suprasegmental aspects of speech analysis such as prosody and intonation contours, consistent with a case described by Coslett et al. (1984).

Deficiencies in FM analysis of tonal stimuli have also been described by Wang et al. (2000) in a PWD patient with a unilateral left hemisphere lesion involving cortical and subcortical white matter of left temporal lobe extending superiorly into frontoparietal regions. Their patient had difficulty in discriminating the directional trajectory (up-going vs. down-going) of pure-tone glides 302 ms in duration as well as 50 ms linear frequency ramps followed by a steady-state tone. These observations are broadly consistent with our findings with formant frequency modulations. Wang et al. (2000) did not utilize a measure of temporal acuity, so it cannot be discerned whether the deficits observed in their case were also independent of more basic problems with temporal resolution.

Neurophysiological and Neuroanatomical Considerations

Overall, our findings provide compelling evidence that prephonemic auditory temporal processing disturbances can occur in PWD secondary to unilateral left temporal lobe lesions and result in substantial problems with auditory comprehension. The dissociation between click fusion and frequency modulation analysis observed in NH cannot readily be accommodated by the concept of a slow clock as suggested by Best and Howard (1994). Rather, the results appear to implicate specialized mechanisms that mediate rapid FM analysis. Evidence from animal neurophysiological studies and human psychophysical experiments suggest that temporally varying sounds undergo specialized analysis involving modulation sensitive neural mechanisms that are distinct from processes underlying the analysis of steady-state sounds (Kay, 1974). These mechanisms or “channels” are not merely concerned with the detection of a change from one frequency to another but are sensitive to the instantaneous temporal properties of frequency change such as the rate, shape, direction, and periodicity of modulation (Kay & Matthews, 1972; Green & Kay, 1973; Collins & Cullen, 1978; Gardner & Wilson, 1979; Regan & Tansley, 1979). They are physiologically distinguishable from analogous mechanisms that process amplitude modulations in sound (Regan & Tansley, 1979; Kay, 1982). The temporal tuning that characterizes the response properties of FM sensitive neurons, their connectivity with other auditory neurons, and their hierarchical organization in the auditory system suggests an intrinsic capacity to track modulations in time.

Frequency modulation sensitive mechanisms have functional characteristics critical to speech reception (Kay, 1982). Studies of the cortical organization of these mechanisms suggest that they are elaborated in the superior temporal cortex in areas confluent with primary auditory cortex and classical language reception areas (Arlinger et al., 1982; Hari & Makela, 1986; Makela et al., 1987). Recent functional magnetic resonance imaging studies have localized FM sensitive mechanisms to so-called belt and parabelt association cortex anterolateral and lateral to Heschl's gyrus (Johnsrude et al., 1997; Binder et al., 2000; Zatorre et al., 2002) in areas that appear to be specialized for processing rapid time varying aspects of sound (Hart et al., 2003). Joanisse and Gati (2003) observed that speech and dynamically varying nonspeech stimuli produce remarkable overlap in neural activation on functional magnetic resonance imaging. Indeed, they suggest that differences appeared to be related to the degree of activation rather than differences in spatial localization.

Interestingly, these areas have been implicated in cortical mapping studies as critical to consonant perception. Examining patients undergoing cortical mapping in preparation for surgical treatment of intractable epilepsy, Boatman et al. (1995) demonstrated that electrical stimulation to lateral mid and posterior superior temporal cortex disrupted the perception of consonant-vowel syllables but not vowels. These regions may form a functional subunit of a posterior stream of auditory processing distributed along the supratemporal cortical plane (Wise et al., 2001).

While there is evidence of bilateral mediation of the speech code, there is growing support from dichotic listening, electrophysiological, neuromagnetic, and functional neuroimaging studies to suggest that there are hemispheric differences in the computational networks that specialize in the analysis of rapid acoustic modulations in speech. Poeppel (2003) has proposed that the neural architecture that analyzes speech signals is asymmetrically analyzed in the time domain, with left-hemisphere mechanisms preferentially extracting information over shorter (25–50 ms) temporal integration windows while right hemisphere mechanisms integrate temporal variations over longer (150–250 ms) windows. Our findings are broadly consistent with this viewpoint. However, the dissociation between click fusion and frequency modulation analysis suggests that the temporal window concept is in need of a higher degree of specification. Specifically, our results suggest that window size may depend on the type of information that is being analyzed in the time domain. Differentiation of auditory objects based on information present in amplitude modulations (on and off) was not affected in our patient with PWD. We would therefore suggest that hemispheric asymmetries are more related to the analysis of rapid spectrotemporal variations that require the tracking of relational structure or temporal patterns in sound.