THE MAN WITH THE PROTEAN MIND
Marcel Kinsbourne was born in Austria in 1931. His family fled the Nazis in 1939, and he spent the remainder of his youth in England. He obtained his Medical degree from Oxford University and later received the British equivalent of a Ph.D. He specialized in pediatric neurology and behavioral neurology and has served on the faculties of Oxford University, Duke University Medical Center, University of Toronto, Harvard Medical School, and Tufts University. He is currently a professor at the New School, a university in New York, where he received an award for Teaching Excellence. He is the author of more than 400 scientific papers, the author or editor of nine books, and has served on the editorial board of 26 scientific journals.
Relationship Between the Central Nervous System and the Conceptual Nervous System
Kinsbourne has spent much of his life questioning, challenging, refuting, and reconstructing several previously accepted ideas about how the brain works. He studies clinical syndromes in patients for clues about brain function and uses his knowledge and discoveries about the brain to devise treatments for neurological disorders. He is also an experimentalist who has invented many paradigms in order to test his theories. Thus, Kinsbourne is both a scientist and a philosopher of science. He moves effortlessly through two levels of neural function: the central nervous system (CNS) and the conceptual nervous system (cns). Within his “cns,” Kinsbourne respects Brodmann’s cytoarchitectonic areas, but acknowledges that functional neural networks are distributed and overlapping both within and across the boundaries of these regions. In a sense, Kinsbourne is the grandfather of what is currently referred to as the cognitive neuroscience view of regional specialization. This view does not attribute functions to one specific brain location, but claims that neural networks are either recruited or inhibited on the basis of competing task demands, changes in arousal, or reaction to damage in the brain. His view of the brain is that of a dynamic organ constantly changing in response to the internal and external environments.
Development of the Notion of Overflow of Activity Between Adjacent Neural Circuits
Kinsbourne (1972, 1974a) was fascinated by the influence of activity in one neural circuit upon another seemingly independent circuit. He demonstrated that when the left hemisphere is occupied with a verbal task (such as memorizing a series of words), visual and auditory attention shifts rightward and the eyes involuntarily move to the right. When primed with a visuospatial task, attention shifts leftward and so do the eyes. He then proved that the converse is also true: rightward orientation improves verbal processing and leftward orientation improves spatial processing.
Depending upon the task or type of stimuli, overflow of activity into adjacent neural circuits can facilitate or interfere with task performance. Elaboration of this novel overflow phenomenon led to the discovery that voices heard by schizophrenics can be inhibited merely by occupying some of the relevant circuits by either widely opening the mouth or humming (Green and Kinsbourne 1990).
Application of Dual Task Methodology Leads to Principle of Functional Cerebral Distance
Kinsbourne elaborated on his theory of hemispheric interaction by examining dual task performance. He created a variety of tasks requiring involvement of neural networks that are either tightly connected to one another within a single hemisphere or widely distributed between the two hemispheres. The two tasks were performed concurrently. For example, Kinsbourne and Cook (1971) asked subjects to balance a dowel rod while repeating sentences (a left hemisphere task) and found that balancing time decreased for the right finger (controlled by left hemisphere) but not the left finger (controlled by right hemisphere). With this “dual task methodology,” they found that young right-handed children already showed the adult pattern of greater disruption of right- rather than left-sided finger tapping when asked to perform oral language or verbal memory tasks (Hiscock et al. 1987). Similarly, as the phonetic difficulty of the verbalizations increase, control of the right hand is increasingly affected. In fact, hand and oral-articulatory neural structures occupy adjoining neocortical space.
These results in both adults and children led Kinsbourne to his principle of functional cerebral distance, which states that the degree of connectivity between two regions predicts dual task performance. For example, while speaking, the ability to simultaneously track, manually sequence, position, or maintain stabilization of the arms and hands is disrupted, particularly on the right side because both verbal ability and control of right-sided motor functions are in the left hemisphere (Kinsbourne and Cook 1971). This paradigm was the first to offer investigators a motor test for laterality, and in various forms it continues to be used for this purpose.
There is reason to suppose that functional cerebral distance increases with age. As networks become pruned and the corpus callosum completes its maturation, incongruent simultaneous processing is able to occur in separate hemispheres better than within a single hemisphere. This makes sense since the number of interhemispheric connections is a fraction of the number of intra-hemispheric connections. This was demonstrated in the study by Merola and Liederman (1985), who showed that children can read upright and inverted letters more accurately when upright letters were presented to one hemisphere and inverted letters to the opposite hemisphere compared to when both letter types were presented to a single hemisphere.
The Developmental Invariance of Cerebral Lateralization
Kinsbourne (1974b) was an early critic of the widely accepted theory of progressive lateralization of cerebral localization of function. Progressive lateralization stated that when a child first develops a skill, it is bilaterally represented in the brain, and with further development, the representation shifts to one hemisphere or the other. Progressive lateralization claimed that the two hemispheres were equipotential at birth and that there was no intrinsic advantage for one hemisphere to predominate in a particular function, such as language, until development of that function (Lenneberg 1967). Evidence for this was based on data that there was equal recovery of language from lesions to either hemisphere in childhood. Kinsbourne (1975) critically reviewed that literature and showed that a) the lesions that were claimed to have been unilateral were secondary to infection and therefore almost certainly bilateral and b) that even at an early age left hemisphere lesions were less well compensated for in terms of language than right hemisphere lesions.
Kinsbourne’s theory of the developmental invariance of cerebral lateralization stated that the two hemispheres have a small but important bias in the way they process inputs that is already established at birth and subsequently elaborated on by experience. Kinsbourne called attention to the rightward bias of the tonic neck reflex in infants which consists of turning the head and eyes sideward, opening the mouth, and pointing the ipsilateral arm in the direction of the gaze. He proposed that the extended hand would develop into the preferred hand for reaching and grasping (Caplan and Kinsbourne 1976). The notion that this bias was genetically mediated was established when Liederman and Kinsbourne (1980) showed that the offspring of two right-handed parents were more likely to exhibit a rightward turning bias in the tonic neck reflex than the offspring of parents with at least one non-right-handed member. This was demonstrated in newborns between 1 and 4 days old, thereby eliminating possible effects of parental handling.
Hiscock and Kinsbourne (1980) reviewed their own and others’ behavioral data and concluded that there was no time at which hemispheric activation swung from symmetry to asymmetry. For example, when right-handers are presented with competing verbal messages to both ears (referred to as dichotic stimulation), they identify more of the right-sided material. When the material is musical, the left ear has the advantage. Children as young as 3 years of age manifest such dichotic listening asymmetrical effects which are as strong as those of older children (Hiscock and Kinsbourne 1977).
The concept of invariance of lateralization with increasing age remains the standard in this field.
The Scaffolding of Circuits Mediating Basic or Reflexive Behavior Evolves into Circuits That Mediate Related Higher Order Behaviors
Kinsbourne promulgated the view that circuits mediating early onset behaviors become the scaffold upon which later onset behaviors were based. For example, he was captivated by the relationship between the onset of right-handed pointing and the onset of babbling. He posited that naming is based on a perceptual change that engages the child’s attention and engenders an orienting response. First words are most often objects of contemplation rather than objects of action. Objects of contemplation are known through orienting (pointing, looking, and turning), whereas objects of action are known through grasping. Naming during the first 2 years occurs as part of an orienting response (almost always occurs with pointing) and orienting is right-biased in right-handers and in the offspring of right-handed people. This association may reinforce the bias to the left hemisphere control of speech very early in life (Kinsbourne and Lempert 1979). More recently, he has pointed out that infant imitation foreshadows entrainment between people as they converse, similar to how a crowd entrains to a unified point of view (Kinsbourne 2005).
Kinsbourne’s Theory of Cerebral Hemispheres as Opponent Systems
Kinsbourne developed a theory of cerebral processes as opponent systems. It is based on the notion that if there is damage to one polar element of the system, symptoms arise that do not occur when both elements are impaired. Areas of cortex that subserve specific functions inhibit other areas that are potentially capable of that same function. Destruction of primarily responsible areas releases homologous areas from inhibition and compensatory functioning is effective in proportion to the severity and extent of the lesion (Kinsbourne 1974b). For example, in left hemispherectomized patients, the right hemisphere is able to compensate for much loss of function because it is free of competitive inhibition from the (absent) left hemisphere. Extrapolating this concept to the control of attention in the normal brain, Kinsbourne suggested that reciprocal inhibition between the hemispheres mediates the balance of attention.
Reconceptualizing the Syndrome Known as Unilateral Neglect as Hemispatial Neglect
Damage to the parietal region of the right hemisphere had been claimed to cause unilateral neglect, a lack of awareness for all stimuli located in the contralateral (left) side of space. Kinsbourne (1987) showed that neglect was not for one side of space, but was actually on a gradient across space and was therefore hemispatial not unilateral. Thus, even when stimuli were clustered in the intact (i.e., right) side of space, the patient with right parietal lobe damage neglected the left-most stimuli (Reuter-Lorenz et al. 1985).
Kinsbourne (1977) posited that hemispatial neglect results in an imbalance in the opponent system that controls lateral orientation with excessive orienting toward the side of the lesion. Kinsbourne explained why right-sided lesions induced more severe neglect than left-sided lesions. He argued that from birth, there is a strong lateral bias to turn rightward mediated by the left hemisphere. Damage to the right parietal lobe diminishes the ability of the right hemisphere to keep this left hemisphere-mediated rightward orientation bias in check.
The concept of unilateral hemispatial neglect as an imbalance of hemisphere activations remains the basis for continuing research into this syndrome.
The Corpus Callosum as an Interhemispheric Activation Equilibrator
Kinsbourne (1974b) was particularly fascinated with the experiments by Levy et al. (1972) in which patients who had surgical section of the interhemispheric commisures were presented with faces composed of two halves of two different familiar faces (chimeric faces). It struck Kinsbourne that these “split-brain” patients never noticed that the faces were odd looking. Instead, when asked to name the person, they spoke the name of the person on the right side of the face. When asked to point, they pointed to the person on the left side of the face. The common interpretation was that this is due to a lack of interhemispheric integration. However, Kinsbourne took this as a demonstration that one hemisphere can gain ascendancy over the other depending upon task demands. He conjectured that the callosum (which was absent in these patients) normally functions as an equilibrator of interhemispheric activation and that its absence in split-brain patients allows extreme shifts in hemispheric activation and wild swings in attention. Kinsbourne (2003) elaborated on the concept of transcallosal equilibration.
Left Hemisphere Specialization for Positive Emotion; Right Hemisphere Specialization for Negative Emotions
Kinsbourne (1986) hypothesized that the left hemisphere mediates focusing on a detail or a single point and is oblivious of everything else. This outlook promotes approach. Kinsbourne pointed out that the right hemisphere is specialized for recognizing and depicting existing relationships and is therefore responsible for establishing context and setting a framework for the point of focal attention. The right hemisphere sees the whole picture, what is really going on, and promotes withdrawal. The approach/withdrawal dichotomy for hemispheric differences is able to accommodate laterality effects for both cognitive and affective processes. He elaborated on this idea to state that the right hemisphere is associated with negative emotions and the left with positive emotions. Kinsbourne and Bemporad (1984) reviewed the literature. They pointed out that patients with left hemisphere damage are often gloomy and depressed, whereas those with right hemisphere damage are often cheerful and elated. Conversely, overactivation of the right hemisphere during seizures causes epileptic patients to cry, whereas left hemisphere seizures induce laughing. In an experiment by Root et al. (2006), participants were presented with happy or angry faces at fixation point, and asked to identify the emotion of each with either their right or left index finger. There were faster response times for angry faces when the left finger was used, indicating right hemisphere dominance for negative emotions, and faster response times for happy faces when the right finger was used, indicating left hemisphere dominance for positive emotions. Kinsbourne’s ideas have been confirmed and elaborated by Davidson in a series of papers which demonstrate that this asymmetry is readily observed specifically within the left vs. right prefrontal cortices (Davidson and Fox 1982; Davidson 2004).
The Dominant Focus of Consciousness and the Notion of Multiple Drafts of Responses
Kinsbourne’s recent work has revolved around developing and refining a unique neural model of consciousness. Dennett and Kinsbourne’s model (1992) rejects the notion that reaction time reflects the sum of the time required for three serial and independent processes: stimulus perception, decision analysis, and response execution. Instead, they propose that every stimulus immediately provokes a stream of responses based on increasing analysis of the situation. Thus, when encountering threatening or dangerous stimuli, an immediate response is often required (if you see a fire, run). Which of the multiple drafts of responses that are prepared is actually executed is influenced by threat level, amount of competing information, competing response demands, and individual differences in what constitutes sufficient support for a response decision. Thus, the combination of interacting neural networks mediating these aspects of decision making determines how fast the response will be and from which part(s) of the brain the dominant activation pattern will emerge.
Given this notion that “the decision maker” is whatever network at a given moment (Kinsbourne 1988) has achieved sufficient activation to dampen down (by lateral inhibition) competing networks, Kinsbourne declared that there is no one seat of consciousness. He states that there is no privileged region that receives and processes information and from which information must be transported. Simultaneously perceiving multiple stimuli and at the same time preparing multiple responses relies on the “winner-takes-all” notion of lateral inhibition. The network with the greatest degree of activation inhibits surrounding networks and therefore becomes the dominant focus. This is an ephemeral process. Within milliseconds, another network can become the most active, and therefore become the dominant focus. The apparently single and unified stream of consciousness is actually composed of many different, largely independent, constantly reforming regional activations. These activations can conflict with or mutually support each other, thereby rapidly shifting the dominant focus, which incorporates the contents of attention.
Kinsbourne’s Argument That There Are No “Multimodal Convergence Zones”
Many theorists including Damasio (1989) argue that information from various points of the brain project upon “multimodal convergence zones” and that conscious awareness emerges from such cortices. However, Kinsbourne forcefully argues that a loss of the ability to simultaneously perceive different modalities or simultaneous (but spatially distributed) stimuli has never been shown to be a consequence of damage to the association cortices. In addition, he argues that the number of meaningful ways in which modalities may be combined is astronomical and well beyond the space available for “association regions.” Instead, he argues that the base state of the brain is largely multimodal and that in real life people are rarely confronted by a single modality situation. In Kinsbourne’s view, it is the simultaneous activation of representations distributed throughout the brain that leads to the unification of neural activity and conscious thought. Cross-modal integration is not accomplished by convergence, but is anchored in the shared topography and timing of its referents. Single modalities are appreciated via an abstraction from the multisensory whole. There is growing evidence that intermodality crosstalk occurs even in the primary areas of the cortices Falchier et al. (2002).
Kinsbourne’s theory of consciousness rests on the idea that the brain is a self-organizing and self-stabilizing network. The brain does not wait idly for stimulation. It is a constantly active network that seeks to maintain equilibrium. Taking this one step further, Kinsbourne (2000) believes that human experience is the direct reflection of the dynamic activity of the brain or “the chatter of neurons.” Subjective awareness is not a product of the brain, but the functioning of the brain itself.
Individual Differences in Criterion Setting for Decision Making
Kinsbourne (2001) theorized that there were individual differences in the amount of information processing required for readiness to make a decision. Individuals with low decision criteria are apt to be impulsive, sensation seeking, and risk taking. This tendency is exemplified by individuals with attention deficit hyperactivity disorder (ADHD). In contrast, individuals with high thresholds for decision making are those that are obsessive compulsive and seek to gather information long past the time needed to inform the decision. Such personality traits as well as their extensions into psychopathology can be seen as arising from the need to self-regulate the overall level of cortical neural activity to an unusually high or low level.
A New Subtype at the Highest Functioning Level of Autistic Spectrum Disorder
The notion that there are individual differences in criterion setting for decision making led Kinsbourne (1991) to identify an apparent subtype of ADHD that he called overfocusing. He defined this disorder in terms of his theory of the brain as a network striving to maintain a homeostatic level of arousal. In contrast to the underfocused person with ADHD, who constantly seeks stimulation so as to raise arousal levels into a subjective comfort zone, the overfocuser’s arousal system continually threatens to overshoot; overfocusers try to dampen arousal by avoiding situations and interactions that are novel or unpredictable. Overfocusers are often diagnosed with ADHD because of their inattention due to persisting concentration on some other topic of interest. Unlike the hyperactive patient who has trouble concentrating, the overfocuser has perseveration of mental set and task orientation. Indeed, overfocusing is on the cusp between the cognitive mainstream and high functioning autism, and an overfocusing factor describes significant properties of autistic behavior (Liss et al. 2006).
In an early collaboration, Marcel Kinsbourne and Elizabeth Warrington set a new standard of experimentation in the analysis of neuropsychological deficits, which ushered in the cognitive neuropsychology movement. They also discovered visual masking by pattern, which is widely used in experiments in which visual stimuli are briefly presented (Kinsbourne and Warrington 1963). Kinsbourne was the first to describe two neurological disorders (Kinsbourne and Warrington 1962; Kinsbourne 1964), the former of which is often called Kinsbourne disease.
In conclusion, Marcel Kinsbourne is truly a man with a protean mind. He has strived throughout his career to think beyond the constraints of popular opinion and accepted theories and has succeeded in restructuring our ideas about the brain to an extent that knows no bounds. What can be a better example than a recent paper titled “Morality without God: Is human brain biology enough?” (Kinsbourne 2000).
Caplan, P. J., & Kinsbourne, M. (1976). Baby drops the rattle: Asymmetry of duration of grasp by infants. Child Development, 47, 532–536.
Damasio, A. R. (1989). Time-locked multiregional retroactivation: A systems-level proposal for the neural substrates of recall and recognition. Cognition, 33(1–2), 25–62.
Davidson, R. J. (2004). What does the prefrontal cortex “do” in affect: Perspectives on frontal EEG asymmetry research. Biological Psychiatry, 67(1–2), 219–233.
Davidson, R. J., & Fox, N. A. (1982). Asymmetrical brain activity discriminates between positive and negative affective stimuli in human infants. Science, 218(4578), 1235–1237.
Dennett, D. C., & Kinsbourne, M. (1992). Time and the observer: The where and when of consciousness in the brain. The Behavioral and Brain Sciences, 15(2), 183–247.
Falchier, A., Clavagnier, S., Barone, P., & Kennedy, H. (2002). Anatomical evidence of multimodal integration in primate striate cortex. The Journal of Neuroscience, 22(13), 5749–5759.
Green, M. F., & Kinsbourne, M. (1990). Subvocal activity and auditory hallucinations: Clues for behavioral treatments. Schizophrenia Bulletin, 16(4), 617–625.
Hiscock, M., & Kinsbourne, M. (1977). Selective listening asymmetry in preschool children. Developmental Psychology, 13, 217–224.
Hiscock, M., & Kinsbourne, M. (1980). Is there a maturational left-right gradient for brain functions? The Behavioral and Brain Sciences, 3, 477.
Hiscock, M., Kinsbourne, M., Samuels, M., & Krause, A. E. (1987). Dual task performance in children: Generalized and lateralized effects of memory encoding up on the rate and variability of concurrent finger tapping. Brain and Cognition, 6, 24–40.
Kinsbourne, M. (1964). Hiatus hernia with contortions of the neck. Lancet, 1(7342), 1058–1061.
Kinsbourne, M. (1972). Eye and head turning indicate cerebral lateralization. Science, 176, 539–541.
Kinsbourne, M. (1974a). Direction of gaze and distribution of cerebral thought processes. Neuropsychologia, 12, 279–281.
Kinsbourne, M. (1974b). Mechanisms of hemispheric interaction in man. In M. Kinsbourne & W. L. Smith (Eds.), Hemispheric disconnection and cerebral function (pp. 260–285). Springfield: Thomas.
Kinsbourne, M. (1975). The ontogeny of cerebral dominance. Annals of the New York Academy of Sciences, 263, 244–250.
Kinsbourne, M. (1977). Hemi-neglect and hemisphere rivalry. In E. A. Weinstein & R. P. Friedland (Eds.), Hemi-inattention and hemisphere specialization (Advances in neurology, pp. 41–49). New York: Raven.
Kinsbourne, M. (1986). Brain organization underlying orientation and gesture: Normal and pathological cases. In J. L. Nespoulous, P. Perron, & A. R. Lecours (Eds.), The biological foundations of gestures: Motor and semiotic aspects (pp. 65–76). Hillsdale: Lawrence Erlbaum.
Kinsbourne, M. (1987). Mechanisms of unilateral neglect. In M. Jeannerod (Ed.), Neurophysiological and neuropsychological aspects of spatial neglect. North Holland: Elsevier Science.
Kinsbourne, M. (1988). Integrated cortical field model of consciousness. In A. J. Marcel & E. Bisiach (Eds.), The concept of consciousness in contemporary science (pp. 239–256). London: Oxford University Press.
Kinsbourne, M. (1991). Overfocusing: An apparent subtype of ADHD. In N. Amir, I. Rapin, & D. Branski (Eds.), Pediatric neurology: Behavior and cognition of the child with brain dysfunction, volume I (Pediatric and Adolescent Medicine, pp. 18–35). Karger: Basel.
Kinsbourne, M. (2000). Morality without God: Is human brain biology enough? Cerebrum, Fall 2000.
Kinsbourne, M. (2001). Dynamic self-organization of the cerebral network. In J. Gotschl (Ed.), Evolution and Progress in democracies: Towards new foundations of a knowledge society. Dordrecht, The Netherlands: Kluwer.
Kinsbourne, M. (2003). The corpus callosum equilibrates the cerebral hemispheres. In E. Zaidel & M. Iacoboni (Eds.), The parallel brain: The cognitive neuroscience of the corpus callosum (pp. 271–278). New York: Academic.
Kinsbourne, M. (2005). Imitation as entrainment: Brain mechanisms and social consequences. In S. Hurley & N. Chater (Eds.), Perspectives on Imitation: From neuroscience to social science (Imitation, human development and culture, Vol. 2, pp. 163–172). Cambridge, MA: MIT Press.
Kinsbourne, M., & Bemporad, B. (1984). Lateralization of emotion: A model and the evidence. In N. A. Fox & R. J. Davidson (Eds.), The psychobiology of affective development. Hillsdale: Lawrence Erlbaum.
Kinsbourne, M., & Cook, J. (1971). Generalized and lateralized effects of concurrent verbalization on a unimanual skill. The Quarterly Journal of Experimental Psychology, 23, 341–345.
Kinsbourne, M., & Lempert, H. (1979). Does left brain lateralization of speech arise from right-biased orienting to salient precepts? Human Development, 22, 270–276.
Kinsbourne, M., & Warrington, E. K. (1962). The effect of an after-coming random pattern on the perception of brief visual stimuli. The Quarterly Journal of Experimental Psychology, 14, 223–234.
Kinsbourne, M., & Warrington, E. (1963). A study of visual perseveration. Journal of Neurology, Neurosurgery, and Psychiatry, 26, 468–475.
Lenneberg, E. (1967). Biological foundations of language. New York: Wiley.
Levy, J., Trevarthen, C., & Sperry, R. W. (1972). Perception of bilateral chimeric figures following hemispheric disconnection. Brain, 95, 61–78.
Liederman, J., & Kinsbourne, M. (1980). Rightward motor bias in newborns depends upon parental right-handedness. Neuropsychologia, 18(4–5), 579–584.
Liss, M., Saulnier, C., Fein, D., & Kinsbourne, M. (2006). Sensory and attention abnormalities in autistic spectrum disorders. Autism, 10, 155–172.
Merola, J. L., & Liederman, J. (1985). Developmental changes in hemispheric independence. Child Development, 56(5), 1184–1194.
Reuter-Lorenz, P. A., Moscovitch, M., & Kinsbourne, M. (1985). Lateral attention biases on a visual line bisection task: Similarities between the performances of neglect patients and normal subjects. Paper to the International Neuropsychological Society meeting, San Diego, CA.
Root, J. C., Wong, P. S., & Kinsbourne, M. (2006). Left hemisphere specialization for response to positive emotional expressions: A divided output methodology. Emotion, 6(3), 473–483.