Neurology of affective prosody and its functional–anatomic organization in right hemisphere

Abstract

Unlike the aphasic syndromes, the organization of affective prosody in brain has remained controversial because affective-prosodic deficits may occur after left or right brain damage. However, different patterns of deficits are observed following left and right brain damage that suggest affective prosody is a dominant and lateralized function of the right hemisphere. Using the Aprosodia Battery, which was developed to differentiate left and right hemisphere patterns of affective-prosodic deficits, functional–anatomic evidence is presented in patients with focal ischemic strokes to support the concepts that (1) affective prosody is a dominant and lateralized function of the right hemisphere, (2) the intrahemispheric organization of affective prosody in the right hemisphere, with the partial exception of Repetition, is analogous to the organization of propositional language in the left hemisphere and (3) the aprosodic syndromes are cortically based as part of evolutionary adaptations underlying human language and communication.

Introduction

Over the last three decades, there has been growing realization that the right hemisphere is essential for language and communication competency and psychological well-being through its ability to modulate affective prosody and gestural behavior, decode connotative (non-standard) word meanings, make thematic inferences, and process metaphor, complex linguistic relationships and non-literal (idiomatic) types of expressions (Benowitz et al., 1983, Borod et al., 1986, Brownell et al., 1984, Brownell et al., 1986, Carton et al., 1999, Cicone et al., 1980, DeKosky et al., 1980, Foldi, 1987, Mitchell and Crow, 2005, Myers, 1999, Ross, 2000, Van Lancker, 1990, Van Lancker and Kempler, 1987, Winner and Gardner, 1977). In fact, the modern studies of the neurological bases underlying prosody (Monrad-Krohn, 1963) and the affective aspects of prosody (Heilman et al., 1975, Ross, 1981, Ross and Mesulam, 1979, Tucker et al., 1977) were all initiated after index patients were evaluated because of complaints concerning substantial psychosocial difficulties after partial recovery from their brain injuries (Heilman, 2002, Monrad-Krohn, 1948; Ross, 1982, Ross, 1997). In addition, functional imaging studies assessing language processing always show, at minimum, bilateral activations of the peri-Sylvian regions when using low-level types of subtraction techniques (Binder et al., 1997, Demonet et al., 2005, Larsen et al., 1978, Petersen et al., 1988, Wildgruber et al., 2002, Zatorre et al., 1992; also see Section 4). Thus, the traditional concept that language is a dominant and lateralized function of the left hemisphere is no longer tenable. This concept evolved from the seminal works of Broca and Wernicke when they described the two fundamental aphasic syndromes observed following focal left but not right hemisphere injury in right-handed individuals (Broca, 1861, Broca, 1865, Eggert, 1977, Lecours and Lhermitte, 1983). In the late 1870s, Hughlings-Jackson (1878–1879) noted that aphasics, even those with dense deficits, were able to communicate their intent through emotional modulation of otherwise impoverished speech and suggested a special role for the right hemisphere in the emotional aspects of communication. The first formal studies of affective communication deficits following right brain damage (RBD),¹ however, were initiated in the mid-1970s (Heilman et al., 1975, Ross and Mesulam, 1979, Tucker et al., 1977) and, shortly thereafter, the concept that aprosodic syndromes are analogous to aphasic syndromes was formalized (Ross, 1981). Since then there has been an increasing number of publications addressing the right hemisphere’s role in modulating the affective aspects of language and communication.

Affective prosody has been conceptualized as a dominant and lateralized function of the right hemisphere (Ross, 1981, Ross and Mesulam, 1979). However, observations to the contrary have been published (Adolphs et al., 2002, Cancelliere and Kertesz, 1990, Ross, 2000). The terms ‘lateralized’ and ‘dominant’ are used interchangeably in the literature although they have somewhat different neurological connotations (Ross, 2000, Ross et al., 1997). A brain function is considered dominant if a unilateral lesion produces a behavioral deficit that subtends both sides of space (Denny-Brown and Banker, 1954, Denny-Brown et al., 1952), a criterion easily met by the various aphasic and aprosodic syndromes. For a function to be strongly lateralized, it must also be shown that the behavioral deficit does not occur following lesions of the opposite hemisphere, as exemplified by the aphasias (Benson, 1979, Broca, 1865). A function may be strongly lateralized but not dominant as exemplified by hemiplegic deficits after forebrain lesions that cause contralateral but not ipsilateral paralysis.

The extent to which affective prosody is lateralized has been more difficult to resolve compared to propositional language functions because various publications have reported considerable disturbances in affective prosody after left brain damage (LBD). Studies in densely aphasic patients found both Comprehension and Production impairments (De Bleser and Poeck, 1985, Schlanger et al., 1976, Seron et al., 1982), bringing into question the original observations by Hughlings-Jackson (1878–1879). Other studies have observed affective communication deficits in LBD patients with minimal or absent aphasic deficits (Cancelliere and Kertesz, 1990, Ross et al., 1997), which run counter to the original observations by Heilman et al., 1975, Tucker et al., 1977 who used mildly aphasic left brain damaged (LBD) patients as lesion comparisons for their RBD patients. Thus, the concept that affective prosody is a dominant and lateralized function of the right hemisphere has been called into question (Cancelliere and Kertesz, 1990, Adolphs et al., 2002). However, an alternative explanation exists for why LBD lesions might disrupt the modulation of affective prosody.

Assuming that affective prosody is a dominant and lateralized function of the right hemisphere, then the process underlying speech Production must entail interhemispheric communication to ensure that the articulatory-verbal and affective-prosodic elements are behaviorally unified and temporally coherent (Klouda et al., 1988, Ross et al., 1997, Speedie et al., 1984). If one wishes to insert anger into a statement, the right hemisphere must be appraised by the left hemisphere of the time it will take to utter the statement so that the intended affective-prosodic information can be matched appropriately with the articulatory output; vice-a-versa, the intended intonation requirements for affective signaling by the right hemisphere could alter the left hemisphere’s plan for articulatory timing. For example, to produce a sarcastic or emphatic statement (Bolinger, 1980), it is often necessary to prolong certain phonetic units to impart the correct attitudinal information. Thus, left hemisphere lesions, especially if they involve deep white matter, could disrupt the higher order integration of affective prosody with the propositional aspects of language causing indirectly a disruption of affective prosody.

In order to test this possibility, the Aprosodia Battery was developed (Ross et al., 1997) in which the verbal-articulatory demands are reduced incrementally when testing subjects on their ability to repeat and comprehend affective prosody. Various emotions are presented using stimuli utterances that are carried first by words (“I am going to the other movies”), then by a repeated monosyllable (“ba ba ba ba ba ba”), and lastly by an asyllabic articulation (“aaaaaahhhh”). In LBD patients with impaired affective prosody, reducing the verbal-articulatory demands caused a robust improvement in their ability to comprehend and repeat affective prosody. Using comparable types of paradigms, similar findings have been reported for affective Comprehension by Tompkins and Flowers, 1985, Lalande et al., 1992 who studied patients within the early phase of long-term recovery and, to a lesser extent, by Pell (2006) who studied patients in the very late post-stroke phase of recovery, approximately 6 years after the ictus.

In RBD patients with impaired affective prosody, reducing the verbal-articulatory demands did not improve their ability to comprehend or repeat affective prosody and, in some instances, actually worsened their performance. More importantly, affective-prosodic deficits in LBD patients were not related to the absence, presence or severity of aphasic deficits, a finding also reported by Geigenberger and Ziegler (2001) for affective Comprehension. The best predictor was if the LBD lesion involved the deep white matter adjacent to the corpus callosum, located below the supplementary motor area and adjacent portions of the anterior cingulate gyrus. The cortical distribution of lesions in LBD patients was also a poor predictor of affective-prosodic disturbances. Based on these findings (Ross et al., 1997), it was suggested that the predominant mechanism underlying affective-prosodic deficits following LBD was loss of callosal integration of the dominant language functions represented in each hemisphere (LBD/Callosal profile) whereas the predominant mechanism underlying affective-prosodic deficits following RBD was loss of affective-communicative representations (Blonder et al., 1991, Bowers et al., 1993, Bowers et al., 1987) and, consequently, loss of the ability to dominantly modulate affective prosody (RBD/Aprosodic profile). An analysis of RBD functional–anatomic relationships, however, was not presented.

Based on earlier lesion work (Gorelick and Ross, 1987, Ross, 1981, Ross and Mesulam, 1979), it was proposed that the functional–anatomic organization of affective prosody in the right hemisphere was analogous to the functional–anatomic organization of propositional language in the left hemisphere. Thus, a syndromatic classification of aprosodias was developed, similar to the aphasias, to indicate different combination of deficits involving Spontaneous affective prosody, affective-prosodic Repetition and affective-prosodic Comprehension. Some subsequent studies have confirmed this functional–anatomic approach while others have not confirmed either the functional or anatomic bases or both (for details see Section 4 and Table 11). The research presented here is a continuation of our inquiry into the neurology of affective prosody using the Aprosodia Battery to quantify deficits (Ross et al., 1997) with the main focus now on right rather than left hemisphere functional–anatomic correlates. In the interim, the Aprosodia Battery has been used to study several different clinical populations with robust results, including patients with fetal and early-life exposure to alcohol (Monnot et al., 2002, Monnot et al., 2001), Alzheimer disease (Testa, Beatty, Gleason, Orbelo, & Ross, 2001), leukoaraiosis (Ross, Hansel, Orbelo, & Monnot, 2005) and schizophrenia (Ross et al., 2001). Because some of the research was focused on elderly populations, requiring the use of appropriate age-matched controls, an unexpected aging effect was encountered in the controls due primarily to impaired Comprehension of affective prosody with increased variability (Orbelo et al., 2005, Orbelo et al., 2003). Since the average age of our stoke patients when first entered into our database has gradually risen over the years from late 50s to mid 60s, the distinct patterns characterizing LBD vs. RBD deficits that were published a decade ago (Ross et al., 1997) need reappraisal. Two main hypotheses will be addressed in this paper: (1) as previously described, patterns of aprosodic deficits following LBD and RBD are different and these patterns remain valid even when using an expanded set of subjects that include elderly individuals and (2) affective prosody is functionally and anatomically organized in the right hemisphere in a manner analogous to propositional language in the left hemisphere. In addition, the following issues will also be addressed and interpreted in the context of our findings: (1) the role of basal ganglia and other non-cortical structures in modulating affective prosody, (2) how recovery over time alters functional–anatomic relationships when attempting to localize functions following focal brain lesions, (3) the inadequacies of functional imaging data in localizing language functions in the brain and (4) the neurobiological basis for lateralization of affective prosody to the right hemisphere.