Implicit Memory in Amnesic Patients: When Is Auditory Priming Spared?
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Journal of the International Neuropsychological Society (1995), 1, 434-442. Copyright © 1995 INS. Published by Cambridge University Press. Printed in the USA. Implicit memory in amnesic patients: When is auditory priming spared? DANIEL L. SCHACTER1 AND BARBARA CHURCH2 1 Harvard University and Memory Disorders Research Center, Veterans Administration Medical Center, Cambridge, MA 02138 2 University of Illinois, Champaign, IL 61820 (RECEIVED February 16, 1995; ACCEPTED March 2, 1995) Abstract Amnesic patients often exhibit spared priming effects on implicit memory tests despite poor explicit memory. In previous research, we found normal auditory priming in amnesic patients on a task in which the magnitude of priming in control subjects was independent of whether speaker's voice was same or different at study and test, and found impaired voice-specific priming on a task in which priming in control subjects is higher when speaker's voice is the same at study and test than when it is different. The present experiments provide further evidence of spared auditory priming in amnesia, demonstrate that normal priming effects are not an artifact of low levels of baseline performance, and provide suggestive evidence that amnesic patients can exhibit voice-specific priming when experimental conditions do not require them to interactively bind together word and voice information. (JINS, 1995, 7, 434-442.) Keywords: Amnesia, Priming, Implicit memory Introduction jects heard a list of spoken words and judged either the category to which each word belongs (semantic encoding It is well known that amnesic patients can exhibit robust task) or the pitch of the speaker's voice (nonsemantic en- implicit memory despite impaired explicit memory. The coding task); half of the speakers were males and half most extensively studied form of implicit memory in am- were females. Subjects then performed an auditory iden- nesic patients is known as direct or repetition priming, tification test in which studied and nonstudied words were where exposure to a word or object influences subsequent presented in white noise and subjects reported what they identification of that item (for review, see Roediger & heard. Half of the studied words were spoken in the same McDermott, 1993; Schacter et al., 1993). Many experi- voice as during the encoding task and half were spoken ments have shown that priming effects can be preserved in a different voice. The experiment revealed equivalent in amnesic patients across a wide variety of materials and amounts of priming in amnesic patients and control sub- tests (for review, see Shimamura, 1986; Bowers & Schac- jects in all experimental conditions. In contrast, amnesics ter, 1993). This finding has been taken as evidence that exhibited a significant impairment on an explicit recog- priming is mediated by a memory system that does not de- nition test that followed the identification test. pend on the medial temporal Iobe/diencephalic structures that are damaged in amnesia (e.g., Gabrieli et al., 1994; These data indicate that auditory priming can be pre- Schacter, 1994; Squire, 1994). served in amnesic patients. Note, however, that priming in both amnesics and controls was unaffected by study- Although most demonstrations of preserved priming to-test changes in speaker's voice—that is, the magnitude in amnesic patients have used visual materials and tests, of priming was nearly identical in the same-voice and we recently reported experiments that examine auditory different-voice conditions for both amnesics and controls. priming in amnesia. In a study by Schacter and colleagues This outcome was not surprising, because previous re- (Schacter et al., 1994), amnesic patients and control sub- search with college students had already shown that prim- ing on the identification-in-noise test is not significantly Reprint requests to: D.L. Schacter, Department of Psychology, Har- influenced by voice change (Schacter & Church, 1992). vard University, 33 Kirkland Street, Cambridge, MA 02138. But other studies of college students have revealed that 434 Spared auditory priming in amnesia 435 study-to-test changes in speaker's voice does influence the of the medial temporal lobe/diencephalic system is to bind magnitude of priming on auditory completion and identi- together the outputs of various different systems and sub- fication tests that do not make use of white noise (Schacter systems (cf. Cohen & Eichenbaum, 1993; Johnson & & Church, 1992; Church & Schacter, 1994). Thus, audi- Chalfonte, 1994; Moscovitch, 1994; Schacter, 1994; tory priming is comprised of a component that is specific Squire, 1994). Although such bound traces normally pro- to speaker's voice as well as a nonspecific component (cf. vide the basis for explicit recall and recognition, Schac- Kirsner et al., 1989). Schacter et al.'s (1994) data suggest ter et al. (1995) suggested that they can also influence that the nonspecific component of auditory priming is implicit test performance. spared in amnesic patients. Schacter et al. (1995) also noted that a similar idea To determine whether the voice-specific component of could be applied to findings of impaired typefont-specific auditory priming is also preserved in amnesics, Schacter priming in Korsakoff amnesics (Kinoshita & Wayland, et al. (1995) used a low-pass filter identification test de- 1993) and impaired priming of novel associations in am- veloped by Church and Schacter (1994). Words presented nesic patients of mixed etiologies (e.g., Schacter & Graf, on this test are degraded by reducing the decibel level of 1986; Shimamura & Squire, 1989). Typefont-specific a distribution of higher frequencies, so that words are priming may require binding between visual features of muffled and hence difficult to identify. Schacter et al. words and abstract orthographic word forms, and prim- (1995) found that control subjects exhibited more priming ing of new associations may require binding between se- when speaker's voice was the same at study and test than mantic and visual features of words. when it was different. In contrast, amnesic patients ex- In summary, one interpretation of extant data on au- hibited similar amounts of priming in same- and different- ditory priming in amnesic patients is that a phonological voice conditions. component of priming that depends on the PRS is pre- Why do amnesic patients exhibit apparently normal served and a voice-specific component that requires levels of nonspecific auditory priming together with im- episodic binding is impaired. However, alternative inter- paired voice-specific priming? We have argued previously pretations of these data are also possible. For example, that auditory priming on completion and identification Ostergaard and Jernigan (1993) have recently argued that tests depends largely on a presemantic perceptual rep- priming is not preserved in amnesic patients. To support resentation system (PRS) that is preserved in amnesic this claim, they have pointed to the existence of impaired patients. The PRS is a collection of cortically-based priming in several studies, nonsignificant trends for prim- domain-specific subsystems that represent information ing impairments in other studies that may have failed to about the form and structure, but not the meaning and detect significant differences because of low statistical associative properties, of words and objects (e.g., Schac- power, and differences in baseline levels of performance ter, 1990,1994; Tulving & Schacter, 1990). With respect between amnesics and controls that can cloud interpre- to auditory priming, we have suggested that two PRS sub- tation of the priming data (but see also Hamman et al., systems may be involved: an auditory word form sub- 1995). Thus, Schacter et al.'s (1995) failure to observe system that represents abstract information about the voice-specific priming in amnesic patients may simply phonological structure of words, and an acoustic subsys- reflect the fact that auditory priming in general is not tem that represents prosodic features of speaker's voice. preserved in amnesic patients. There may be no need to The former subsystem, we contended, subserves the com- postulate, as Schacter et al. (1995) did, that one kind of ponent of priming that is insensitive to changes in speaker's auditory priming is preserved in amnesic patients and an- voice, while the latter subsystem subserves priming effects other kind is impaired. The observation of normal prim- that are sensitive to changes in speaker's voice. ing by Schacter et al. (1994) may have limited generality, Our finding that amnesics exhibit normal auditory or might even be an unreplicable phenomenon. priming on the identification-in-noise test (Schacter et al., To address these issues, and to provide more informa- 1994), which failed to yield evidence of voice-specific tion about the voice-specific component of priming in am- priming even in our control subjects, suggests that the nesic patients, we describe two experiments that examine phonological word form subsystem of PRS is preserved auditory priming in amnesics and controls. One purpose in amnesia. In contrast, the absence of voice-specific of these experiments is to determine whether amnesic pa- priming in amnesics (Schacter et al., 1995) led us to sug- tients can exhibit voice-specific priming under conditions gest that in order to exhibit voice specific priming on the in which voice-specific effects do not require binding filter identification test under the conditions of our exper- between words and voices. In the Schacter et al. (1995) iments, it may be necessary to bind together phonolog- experiment, all of the voices that were used on the filter ical information concerning a spoken word form and identification test had already appeared on the study list. acoustic information concerning the voice of the speaker Thus, all of the test voices were equally familiar to the enunciating the word. Furthermore, such binding may re- subjects, and voice-specific priming could be exhibited quire the participation of medial temporal lobe/dience- only when subjects had retained a specific association be- phalic structures that are damaged in amnesic patients.