A Common Neural Substrate for Language Production and Verbal Working Memory

Verbal working memory (VWM), the ability to maintain and manipulate representations of speech sounds over short periods, is held by some influential models to be independent from the systems responsible for language production and comprehension [e.g., Baddeley, A. D. Working memory, thought, and action. New York, NY: Oxford University Press, 2007]. We explore the alternative hypothesis that maintenance in VWM is subserved by temporary activation of the language production system [Acheson, D. J., & MacDonald, M. C. Verbal working memory and language production: Common approaches to the serial ordering of verbal information. Psychological Bulletin, 135, 50–68, 2009b]. Specifically, we hypothesized that for stimuli lacking a semantic representation (e.g., nonwords such as mun), maintenance in VWM can be achieved by cycling information back and forth between the stages of phonological encoding and articulatory planning. First, fMRI was used to identify regions associated with two different stages of language production planning: the posterior superior temporal gyrus (pSTG) for phonological encoding (critical for VWM of nonwords) and the middle temporal gyrus (MTG) for lexical–semantic retrieval (not critical for VWM of nonwords). Next, in the same subjects, these regions were targeted with repetitive transcranial magnetic stimulation (rTMS) during language production and VWM task performance. Results showed that rTMS to the pSTG, but not the MTG, increased error rates on paced reading (a language production task) and on delayed serial recall of nonwords (a test of VWM). Performance on a lexical–semantic retrieval task (picture naming), in contrast, was significantly sensitive to rTMS of the MTG. Because rTMS was guided by language production-related activity, these results provide the first causal evidence that maintenance in VWM directly depends on the long-term representations and processes used in speech production.

[1]  Fahmeed Hyder,et al.  Neurophysiology of functional imaging , 2009, NeuroImage.

[2]  Daniel J. Acheson,et al.  Areas of left perisylvian cortex mediate auditory–verbal short-term memory , 2011, Neuropsychologia.

[3]  Roland Sparing,et al.  Enhancing Picture Naming with Transcranial Magnetic Stimulation , 2006, Behavioural neurology.

[4]  T. Paus,et al.  Seeing and hearing speech excites the motor system involved in speech production , 2003, Neuropsychologia.

[5]  Caroline Catmur,et al.  Auditory Short-term Memory Capacity Correlates with Gray Matter Density in the Left Posterior STS in Cognitively Normal and Dyslexic Adults , 2011, Journal of Cognitive Neuroscience.

[6]  Yoshio Takane,et al.  Epoch-specific functional networks involved in working memory , 2013, NeuroImage.

[7]  Shira Katseff,et al.  Brain regions underlying repetition and auditory-verbal short-term memory deficits in aphasia: Evidence from voxel-based lesion symptom mapping , 2012, Aphasiology.

[8]  R. Töpper,et al.  Facilitation of picture naming after repetitive transcranial magnetic stimulation , 1999, Neurology.

[9]  B. Postle Working memory as an emergent property of the mind and brain , 2006, Neuroscience.

[10]  William W. Graves,et al.  Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies. , 2009, Cerebral cortex.

[11]  Daniel J. Acheson,et al.  Twisting tongues and memories: Explorations of the relationship between language production and verbal working memory. , 2009, Journal of memory and language.

[12]  Felix M Mottaghy,et al.  Bilateral parieto‐frontal network for verbal working memory: an interference approach using repetitive transcranial magnetic stimulation (rTMS) , 2002, The European journal of neuroscience.

[13]  Charles Hulme,et al.  Concrete words are easier to recall than abstract words: Evidence for a semantic contribution to short-term serial recall. , 1999 .

[14]  A D Friederici,et al.  Phonological processing during language production: fMRI evidence for a shared production-comprehension network. , 2003, Brain research. Cognitive brain research.

[15]  J. Fiez,et al.  Functional Magnetic Resonance Imaging (fmri) Was Used to Investigate the Neural Substrates of Component Processes in Verbal Working Memory. Based on Behavioral Research Using , 2022 .

[16]  Susan M. Ravizza,et al.  Left TPJ activity in verbal working memory: Implications for storage- and sensory-specific models of short term memory , 2011, NeuroImage.

[17]  Gregory Hickok,et al.  Neural correlates of word production stages delineated by parametric modulation of psycholinguistic variables , 2009, Human brain mapping.

[18]  Thomas J. Grabowski,et al.  The Left Posterior Superior Temporal Gyrus Participates Specifically in Accessing Lexical Phonology , 2008, Journal of Cognitive Neuroscience.

[19]  N. Cowan Attention and Memory: An Integrated Framework , 1995 .

[20]  M. Hallett,et al.  Induction of a recall deficit by rapid-rate transcranial magnetic stimulation. , 1994, Neuroreport.

[21]  G D Brown,et al.  Word-frequency effects on short-term memory tasks: evidence for a redintegration process in immediate serial recall. , 1997, Journal of experimental psychology. Learning, memory, and cognition.

[22]  Michael S. Humphreys,et al.  Articulatory loop explanations of memory span and pronunciation rate correspondences: A cautionary note , 1988 .

[23]  John E. Desmond,et al.  Enhancement of Phonological Memory Following Transcranial Magnetic Stimulation (TMS) , 2006, Behavioural neurology.

[24]  Bradley R. Postle,et al.  Distraction-spanning sustained activity during delayed recognition of locations , 2006, NeuroImage.

[25]  J. Jonides,et al.  Overlapping mechanisms of attention and spatial working memory , 2001, Trends in Cognitive Sciences.

[26]  Paul Boersma,et al.  Praat, a system for doing phonetics by computer , 2002 .

[27]  Richard S. J. Frackowiak,et al.  The neural correlates of the verbal component of working memory , 1993, Nature.

[28]  Bradley R. Postle,et al.  Localization of load sensitivity of working memory storage: Quantitatively and qualitatively discrepant results yielded by single-subject and group-averaged approaches to fMRI group analysis , 2007, NeuroImage.

[29]  M. Seghier,et al.  The left superior temporal gyrus is a shared substrate for auditory short-term memory and speech comprehension: evidence from 210 patients with stroke , 2009, Brain : a journal of neurology.

[30]  Richard C. Atkinson,et al.  Human Memory: A Proposed System and its Control Processes , 1968, Psychology of Learning and Motivation.

[31]  Jarrod A. Lewis-Peacock,et al.  Temporary Activation of Long-Term Memory Supports Working Memory , 2008, The Journal of Neuroscience.

[32]  E. Capaldi,et al.  The organization of behavior. , 1992, Journal of applied behavior analysis.

[33]  Emrah Düzel,et al.  Verbal working memory components can be selectively influenced by transcranial magnetic stimulation in patients with left temporal lobe epilepsy , 1996, Neuropsychologia.

[34]  A. Baddeley Working Memory, Thought, and Action , 2007 .

[35]  Michael Erb,et al.  Language aptitude for pronunciation in advanced second language (L2) Learners: Behavioural predictors and neural substrates , 2013, Brain and Language.

[36]  Tracy R. Henderson,et al.  Simple metric for scaling motor threshold based on scalp-cortex distance: application to studies using transcranial magnetic stimulation. , 2005, Journal of neurophysiology.

[37]  Giulio Tononi,et al.  The Neural Bases of the Short-Term Storage of Verbal Information Are Anatomically Variable across Individuals , 2007, The Journal of Neuroscience.

[38]  Daniel J. Acheson,et al.  Verbal working memory and language production: Common approaches to the serial ordering of verbal information. , 2009, Psychological bulletin.

[39]  Michael J. Watkins,et al.  Serial recall and the modality effect: Effects of word frequency. , 1977 .

[40]  Bradley R. Buchsbaum,et al.  The Search for the Phonological Store: From Loop to Convolution , 2008, Journal of Cognitive Neuroscience.

[41]  Katie L. McMahon,et al.  Independent Distractor Frequency and Age-of-Acquisition Effects in Picture–Word Interference: fMRI Evidence for Post-lexical and Lexical Accounts according to Distractor Type , 2012, Journal of Cognitive Neuroscience.

[42]  W. Levelt,et al.  The spatial and temporal signatures of word production components , 2004, Cognition.

[43]  M. Pickering,et al.  Do people use language production to make predictions during comprehension? , 2007, Trends in Cognitive Sciences.

[44]  R. Berndt,et al.  Working memory retention systems: a state of activated long-term memory. , 2003, The Behavioral and brain sciences.

[45]  G S Dell,et al.  A spreading-activation theory of retrieval in sentence production. , 1986, Psychological review.

[46]  E. Wassermann Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the International Workshop on the Safety of Repetitive Transcranial Magnetic Stimulation, June 5-7, 1996. , 1998, Electroencephalography and clinical neurophysiology.

[47]  G. Buzsáki Rhythms of the brain , 2006 .

[48]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[49]  Rebecca Treiman,et al.  The English Lexicon Project , 2007, Behavior research methods.

[50]  Nadine Martin Eleanor M. Saffran Language and Auditory-verbal Short-term Memory Impairments: Evidence for Common Underlying Processes , 1997 .

[51]  Charles Hulme,et al.  Effects of word frequency and age of acquisition on short-term memory span , 1994, Memory & cognition.

[52]  Dennis Norris,et al.  Speech errors and the phonological similarity effect in short-term memory: Evidence suggesting a common locus , 2007 .

[53]  R. Schweickert A multinomial processing tree model for degradation and redintegration in immediate recall , 1993, Memory & cognition.

[54]  B. Rossion,et al.  Revisiting Snodgrass and Vanderwart's Object Pictorial Set: The Role of Surface Detail in Basic-Level Object Recognition , 2004, Perception.

[55]  Robert G. Crowder,et al.  The locus of the lexicality effect in short-term memory for phonologically identical lists , 1976 .

[56]  Costanza Papagno,et al.  The Neural Correlates of Phonological Short-term Memory: A Repetitive Transcranial Magnetic Stimulation Study , 2006, Journal of Cognitive Neuroscience.

[57]  Randi C. Martin,et al.  Independence of Input and Output Phonology in Word Processing and Short-Term Memory , 1999 .

[58]  K. Oberauer Access to information in working memory: exploring the focus of attention. , 2002, Journal of experimental psychology. Learning, memory, and cognition.

[59]  F. M. Mottaghy,et al.  Facilitation of picture naming by focal transcranial magnetic stimulation of Wernicke’s area , 1998, Experimental Brain Research.