Enhanced physiologic discriminability of stop consonants with prolonged formant transitions in awake monkeys based on the tonotopic organization of primary auditory cortex

Abstract

Many children with specific language impairment (SLI) have difficulty in perceiving stop consonant-vowel syllables (e.g., /ba/, /ga/, /da/) with rapid formant transitions, but perform normally when formant transitions are extended in time. This influential observation has helped lead to the development of the auditory temporal processing hypothesis, which posits that SLI is causally related to the processing of rapidly changing sounds in aberrantly expanded windows of temporal integration. We tested a potential physiological basis for this observation by examining whether syllables varying in their consonant place of articulation (POA) with prolonged formant transitions would evoke better differentiated patterns of activation along the tonotopic axis of A1 in awake monkeys when compared to syllables with short formant transitions, especially for more prolonged windows of temporal integration. Amplitudes of multi-unit activity evoked by /ba/, /ga/, and /da/ were ranked according to predictions based on responses to tones centered at the spectral maxima of frication at syllable onset. Population responses representing consonant POA were predicted by the tone responses. Predictions were stronger for syllables with prolonged formant transitions, especially for longer windows of temporal integration. Relevance of findings to normal perception and that occurring in SLI are discussed.

Introduction

In one of the most influential and controversial observations in phonology, Tallal et al. have reported that many children with specific language impairment (SLI) had difficulty in the perception of stop consonant-vowel (CV) syllables (e.g., /ba/, /ga/, /da/) with rapid formant transitions (e.g., 40 ms), but performed similarly to controls when formant transitions were extended in time (e.g., 80 ms) (for reviews see Tallal et al., 1993, Tallal, 2004). This fundamental observation has been replicated (e.g., Elliott et al., 1989, Kraus et al., 1996, Stark and Heinz, 1996; for review see Burlingame et al., 2005) and expanded to include both subjects with dyslexia and with deficits in other, non-linguistic, auditory perceptions that involve processing of rapidly changing sound stimuli (e.g., Hari and Kiesilä, 1996, Wright et al., 1997, Helenius et al., 1999, Laasonen et al., 2000, King et al., 2003). Ultimately, this evolving and frequently contradictory body of evidence led to the formulation of the auditory temporal processing hypothesis, which posit that difficulties in processing rapidly changing sound stimuli is causally related to SLI (Tallal, 2004). In its latest form, individuals with SLI exhibit deficiencies in phonological functions because they aberrantly process rapidly changing sound stimuli in expanded temporal windows of integration, “chunking” acoustic events together in time periods too large to allow the fine-grained patterns of speech to be readily discriminated. This hypothesis has become so influential that it has spawned commercially available and clinically successful remediation programs (Merzenich et al., 1996, Tallal et al., 1996, Tallal et al., 1998, Tallal, 2004; see also Kujala et al., 2001, Stevens et al., 2008).

While the temporal processing hypothesis remains highly contentious (e.g., Studdert-Kennedy and Mody, 1995, Bishop et al., 1999, Goswami, 2003), temporal or other auditory processing deficits are likely causal in a subset of people with SLI (Heath et al., 1999, Habib, 2000, Ramus et al., 2003). Strong evidence that temporal processing deficits are directly relevant to SLI was provided by Benasich and Tallal (2002), who found that performance in 6–9 months infants on a rapid auditory discrimination task was predictive of later language impairments at 2 and 3 years of age. While not a demonstration of causality, this result does suggest that auditory processing plays an important role in the maturation of speech functions. Furthermore, this finding is consistent with modern views of developmental disorders, according to which fundamental deficits in neural processing (e.g., auditory temporal processing), often produced by a genetic anomaly, may only be reliably identified at early developmental stages (Karmiloff-Smith, 1998, see also Goswami, 2003). At later developmental stages, these early deficits may be partially ameliorated by compensatory mechanisms and yet result in more persistent, and higher-order deficiencies (e.g., SLI).

What remains unresolved in the consideration of these larger issues is the question of why some children with SLI perceive stop CVs with longer formant transitions more accurately than those with short formant transitions. Simply stating that the cause is a deficit in rapid temporal processing does not help to identify potential neural substrates of SLI. This issue is extremely important, as illuminating neural mechanisms potentially relevant for the improvement in phonetic discrimination might provide valuable insights into the competing hypotheses regarding the etiology of SLI and encourage modifications of remediation strategies. Thus, in order to more fully examine this question at a physiological level, data and hypotheses that directly address the differential perception of stop CV syllables must be incorporated into any explanatory framework for SLI.

Almost as contentious as the temporal processing hypothesis of SLI are the competing ideas regarding the perception of stop consonants. At one extreme, their perception is thought to be accomplished through a specialized, speech-specific module that reacquires the intended phonetic gestures of the speaker (e.g., Liberman et al., 1967, Liberman and Mattingly, 1985). Thus, speech perception is intimately tied to speech production. At the other extreme, general principles of auditory processing are thought to be sufficient to map the acoustic signal onto discrete phonetic categories (e.g., Lotto and Kluender, 1998, Stevens, 1980, Kuhl, 2004). This hypothesis is further supported by evidence that humans and non-human animals share many similarities in speech perception (e.g., Kuhl, 1986, Lotto et al., 1997, Ramus et al., 2000, Sinnott and Gilmore, 2004). These similarities justify the use of non-human animal models to examine some of the fundamental questions concerning physiological mechanisms of speech perception.

One of the most prominent acoustically-based hypotheses put forth to explain perceptual differences in stop consonants argue that the short-term acoustic spectrum within the first 20 ms of consonant onset (release) is a major determinant of their differential perception (Stevens and Blumstein, 1978, Blumstein and Stevens, 1979, Blumstein and Stevens, 1980, Chang and Blumstein, 1981). According to this hypothesis, onset spectra that are diffuse and display maxima at higher frequencies (diffuse rising) promote the perception of /d/, those that are diffuse and display maxima at lower frequencies (diffuse falling) promote the perception of /b/, while more compact spectra with maxima at mid-frequencies promote the perception of /g/. While modifications of this basic scheme have been made that incorporate the onset spectra at consonant onset within the context of later acoustic spectra occurring during the following vowel (e.g., Lahiri et al., 1984), the preceding explanation works well when onset spectra are not ambiguous (Alexander and Kluender, 2008). Furthermore, onset spectra are sufficient for stop consonant discrimination in neonates, children, and adults when stimuli are exceedingly short and lack prolonged vowels (<50 ms), or when formant transitions are omitted from the synthesized syllables (Bertoncini et al., 1987, Ohde et al., 1995, Ohde and Halay, 1997, Ohde and Abou-Khalil, 2001). Overall, these results support the importance of onset spectra in the perception of stop consonants varying in their place of articulation (POA).

An attractive feature of this perceptual hypothesis is that it provides a physiologically plausible means by which stop consonants can be differentially represented at early stages of auditory cortical processing. Multiple studies have shown that complex vocalizations are differentially represented in primary auditory cortex (A1) of experimental animals based on the underlying tonotopic organization and the spectral content of the sounds (e.g., Creitzfeldt et al., 1980, Wang et al., 1995, Steinschneider et al., 2003, Mesgarani et al., 2008). This relationship between stop consonant spectra and tonotopic patterns of activity in A1 implies that activation by /b/ should be maximal in low best frequency (BF) regions of A1, while /g/ and /d/ should maximally excite mid- and high-BF regions of A1, respectively. Physiological results in A1 support this prediction when examining onset responses evoked by stop CV syllables (Steinschneider et al., 1995, Engineer et al., 2008).

Integrating the perceptual hypothesis of Stevens and Blumstein (1978) with both the physiological characteristics of A1 noted above and the temporal processing hypothesis of SLI leads to the two predictions that are the focus of this report. First, syllables with prolonged formant transitions should evoke better-differentiated patterns of activation along the A1 tonotopic axis when compared to syllables with short formant transitions. This prediction is based on the premise that one consequence of lengthening formant transitions is to prolong the duration of spectral differences between the consonants prior to their convergence to common steady-state values. Second, the enhanced response differentiation for prolonged formant transition syllables relative to syllables with rapid formant transitions should be most evident when neural activity is analyzed within longer windows of temporal integration. This work expands our previous examination of POA representation in monkey A1, which only examined neural responses within the first 35 ms after stimulus onset (short temporal integration window) and only to syllables with 40 ms formant transitions (Steinschneider et al., 1995).