The Influence of Explicit Instructions and Stimulus Material on Lateral Frontal Responses to an Encoding Task

In this functional magnetic resonance imaging study, we explored the effects of both stimulus material and encoding task demands on activation in lateral prefrontal cortex (PFC). Two factors were manipulated: material type and task instructions. Subjects encoded words or abstract figures (factor 1: stimulus type) and were required to make either a meaning-based or a form-based (letter or shape) decision about each stimulus (factor 2: task instructions). Abstract figures engendered significantly higher levels of right PFC activity than did words. This effect was seen for meaning-based and form-based processing tasks and was significantly greater for the former. We did not observe a differential response of left lateral PFC to verbal and pictorial material. A double dissociation, however, was found within left PFC. A ventrolateral region (within left inferior frontal gyrus) showed the highest levels of activity when words were processed according to their meaning whereas activity in a more dorsolateral region (within left middle frontal gyrus) was greatest when words were processed according to their form (constituent letters). We have therefore observed a main effect of material type in producing lateralized activation of frontal lobes, although the strength of this effect is sensitive to the nature of the task that subjects are asked to perform. Left-side lateral PFC activity is also sensitive to task instructions but this effect was specific to verbal material. The complex patterns of frontal effect counsel against any simple dichotomy of frontal function at the level of either material or task type.

[1]  Edward E. Smith,et al.  Working memory in humans: Neuropsychological evidence. , 1995 .

[2]  J. Desmond,et al.  Material‐specific lateralization of prefrontal activation during episodic encoding and retrieval , 1998, Neuroreport.

[3]  Irene P. Kan,et al.  Effects of Repetition and Competition on Activity in Left Prefrontal Cortex during Word Generation , 1999, Neuron.

[4]  Karl J. Friston,et al.  Willed action and the prefrontal cortex in man: a study with PET , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[5]  Edward E. Smith,et al.  Working Memory: A View from Neuroimaging , 1997, Cognitive Psychology.

[6]  J. Jonides,et al.  Dissociating verbal and spatial working memory using PET. , 1996, Cerebral cortex.

[7]  M. Petrides,et al.  Specialized systems for the processing of mnemonic information within the primate frontal cortex. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[8]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[9]  Alan A. Wilson,et al.  Neuroanatomical correlates of encoding in episodic memory: levels of processing effect. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[10]  M. Farah,et al.  Role of left inferior prefrontal cortex in retrieval of semantic knowledge: a reevaluation. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[11]  A R McIntosh,et al.  Neural correlates of the episodic encoding of pictures and words. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[12]  Richard S. J. Frackowiak,et al.  Functional anatomy of a common semantic system for words and pictures , 1996, Nature.

[13]  P. Goldman-Rakic,et al.  Activation of human prefrontal cortex during spatial and nonspatial working memory tasks measured by functional MRI. , 1996, Cerebral cortex.

[14]  J. Desmond,et al.  The role of left prefrontal cortex in language and memory. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[15]  P. Goldman-Rakic,et al.  Human Brain Mapping 6:14–32(1998) � Dissociation of Mnemonic and Perceptual Processes During Spatial and Nonspatial Working Memory Using fMRI , 2022 .

[16]  R. Henson,et al.  Frontal lobes and human memory: insights from functional neuroimaging. , 2001, Brain : a journal of neurology.

[17]  A. Owen The Functional Organization of Working Memory Processes Within Human Lateral Frontal Cortex: The Contribution of Functional Neuroimaging , 1997, The European journal of neuroscience.

[18]  C. Stern,et al.  Prefrontal–Temporal Circuitry for Episodic Encoding and Subsequent Memory , 2000, The Journal of Neuroscience.

[19]  P. Goldman-Rakic The prefrontal landscape: implications of functional architecture for understanding human mentation and the central executive. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[20]  Karl J. Friston,et al.  Spatial registration and normalization of images , 1995 .

[21]  T. Robbins,et al.  The prefrontal cortex: Executive and cognitive functions. , 1998 .

[22]  P. T. Fox,et al.  Positron emission tomographic studies of the cortical anatomy of single-word processing , 1988, Nature.

[23]  S. Petersen,et al.  Practice-related changes in human brain functional anatomy during nonmotor learning. , 1994, Cerebral cortex.

[24]  B. Postle,et al.  Maintenance versus Manipulation of Information Held in Working Memory: An Event-Related fMRI Study , 1999, Brain and Cognition.

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

[26]  Alan C. Evans,et al.  BrainWeb: Online Interface to a 3D MRI Simulated Brain Database , 1997 .

[27]  R. Passingham,et al.  Specialisation within the prefrontal cortex: the ventral prefrontal cortex and associative learning , 2000, Experimental Brain Research.

[28]  S. Petersen,et al.  Hemispheric Specialization in Human Dorsal Frontal Cortex and Medial Temporal Lobe for Verbal and Nonverbal Memory Encoding , 1998, Neuron.

[29]  Marcia K. Johnson,et al.  The role of prefrontal cortex during tests of episodic memory , 1998, Trends in Cognitive Sciences.

[30]  Edward Awh,et al.  Spatial versus Object Working Memory: PET Investigations , 1995, Journal of Cognitive Neuroscience.

[31]  P. Goldman-Rakic The prefrontal landscape: implications of functional architecture for understanding human mentation and the central executive. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[32]  R. Dolan,et al.  Active representation of shape and spatial location in man. , 1996, Cerebral cortex.

[33]  T. Shallice,et al.  “Sculpting the Response Space”—An Account of Left Prefrontal Activation at Encoding , 2000, NeuroImage.

[34]  R N Henson,et al.  Depth of processing effects on neural correlates of memory encoding: relationship between findings from across- and within-task comparisons. , 2001, Brain : a journal of neurology.

[35]  E. Bizzi,et al.  The Cognitive Neurosciences , 1996 .

[36]  Leslie G. Ungerleider,et al.  Face encoding and recognition in the human brain. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[37]  Alan D. Baddeley,et al.  THE TROUBLE WITH LEVELS: A REEXAMINATION OF CRAIK AND LOCKHART'S FRAMEWORK FOR MEMORY RESEARCH , 1978 .

[38]  C. D. Frith,et al.  The Role of the Dorsolateral Prefrontal Cortex in Random Number Generation: A Study with Positron Emission Tomography , 2000, NeuroImage.

[39]  Edward E. Smith,et al.  Dissociation of Storage and Rehearsal in Verbal Working Memory: Evidence From Positron Emission Tomography , 1996 .

[40]  F. Craik,et al.  Hemispheric encoding/retrieval asymmetry in episodic memory: positron emission tomography findings. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[41]  Jordan Grafman,et al.  Handbook of Neuropsychology , 1991 .

[42]  M Petrides,et al.  Impairments on nonspatial self-ordered and externally ordered working memory tasks after lesions of the mid-dorsal part of the lateral frontal cortex in the monkey , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[43]  A. Dale,et al.  Building memories: remembering and forgetting of verbal experiences as predicted by brain activity. , 1998, Science.