THE ONTOGENY AND ASYMMETRY OF THE HIGHEST BRAIN SKILLS AND THE PATHOGENESIS OF SCHIZOPHRENIA

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Publication Date:
February 28, 2013

Vadim S. Rotenberg

E-mail: vadir@post.tau.ac.il

Abarbanel Mental Health Center, Bat-Yam 59100, Israel.

BEHAVIORAL AND BRAIN SCIENCES (2004) 27:6
Commentary /Burns: Cortical connectivity, metarepresentation, and the social brain: The ontogeny and asymmetry of the highest brain skills and the pathogenesis of schizophrenia

Abstract: The most developed and the latest-to-mature mental skills represented in the creation of mono- versus polysemantic contexts are related respectively to the left and right frontal lobe. A polysemantic way of thinking is responsible for the subject's successful integration in the polydi-mensional world. The functional insufficiency of this right-hemispheric way of thinking displays a predisposition toward the development of mental disorders, including schizophrenia.

I agree with the main messages of the target article, that schizophrenia is a disorder of the social brain, that the development of this disease is related to the disturbed frontoparietal and fron-totemporal connectivity, and that some peculiar features of human ontogenesis predispose subjects to these disturbances of connectivity. However, one important point is missed, related to the ontogeny and function of the orbitofrontal asymmetry.

The disturbance of this area does not cause definite and well-traceable single signs, like apraxia, spatial hemineglect, and so on. In contrast to these relatively local disorders, right anterior insult has interfered with the ability to explore an image in an organized fashion and with the more global functions like empathy, theory of mind, sense of self (Craik et al. 1999; Devinsky 2000; Keenan et al. 2001; Schore 2003; Shamay-Tsoory et al. 2003).

I suggest that in the most general form, the difference between two strategies of thinking related to the frontal functions of the left- and right hemispheres is reduced to opposite modes of organizing the contextual connection between elements of information (Rotenberg 1979; 1982; 1985; 1993; 2004; Rotenberg & Arshavsky 1979). Left-hemisphere frontal pole so organizes any sign material (whether symbolic or iconic) as to create a strictly ordered and unambiguously understood monosemantic context. The formation of this context requires an active choice from the many real and potential connections between the multiform objects and phenomena of a few definite connections that would facilitate an ordered analysis, building a pragmatically convenient but simplified and restricted model of reality based on probability forecasting and cause-and-effect relations.

In contrast, the function of the symmetrical structure of the right hemisphere is a simultaneous capture of an infinite number of connections and the formation of an integral, but ambiguous, polysemantic context. In such a context, the whole is determined by the interconnections between its elements that interact with each other on many semantic planes simultaneously, like images in dreams. Understanding of metaphors and sense of humor are dependent on the right hemisphere (Wapner et al. 1981; Winner & Gardner 1977).

These two types of context complete each other and have sense only in comparison with one another. For the right hemisphere disconnected from the left one, the world is holistic but not polysemantic. However, these types of context are not equal, because the polysemantic view on the world, although being opposite to the monosemantic one, actually includes the latter as a component, while the converse is not true. Polysemantic thinking is the highest human mental function, responsible for creativity and integration of past, present, and future experience (Wheeler et al. 1997). Great apes lack even the initial precursors of polysemantic thinking.

The advantage of the right frontal brain corresponds to the more prominent arborization of the neural net (Saugstad 1998) and to the activation of a much broader net of associations in comparison to the left hemisphere (Beeman et al. 1994; Chiarello 1998; Coney & Evans 1999).

Brain maturation starts with faster overall growth of the right hemisphere in the first years after birth, interrupted by the left hemisphere maturation gradient, followed by another shift to a leading role of the right hemisphere in early adolescence. The frontal lobes and particularly the right frontal lobe structures and connections are the last regions to mature (Thatcher et al. 1987; Saugstad 1998).

In the frame of the theory of contexts, this schedule of maturation has a following explanation: The main functions of the right hemisphere that precede the development of the polysemantic way of thinking (the ability to grasp the reality as a whole; the emotional attachment to the mother [Schore 2003]; the regulation of the withdrawal behavior in the inappropriate conditions [Davidson 1992]; the integration of affect, behavior and autonomic activity [Schore 2003]) are the basic functions of survival (Saugstad 1998), and for this reason they are the first to appear. In the next crucial stage of the development, a process of differentiation of the elements of reality appears: a distinguishing of self from the environment, the ability to analyze cause-and-effect relationships, the orientation in the time vector, and finally the creation of the conscious model of the reality and of self-concept. This process of differentiation requires the expertise of the left hemisphere and its ability to form a monosemantic context.

However, to be comfortably integrated in the polydimensional world and to cope with all contradictions, a subject has to overcome, on a new level, the restrictions of the monosemantic model that is included in the more broad polysemantic picture.

Females are characterized by earlier brain maturation (i.e., achieving the final point of maturation sooner) than males. In general, the longer the process of maturation, the higher the level ol brain structure development achieved. This may be a reason why males more often display outstanding creativity (Saugstad 1998). However, the increased duration of maturation in males makes the right hemisphere more sensitive and vulnerable to any alterative influences and may cause its functional insufficiency that displays a predisposition to different forms of pathology, including schizophrenia (Rotenberg 1979; 1982; 1995; Schore 2003).

Cutting (1992) proposed that schizophrenic patients with a preponderance of negative symptoms display right-hemisphere dysfunction. In schizophrenic patients, the right hemisphere is no more dominant in the functions it usually controls in normal subjects: perception of facial emotions (Borocl et al. 1993), visuospa-tial task performance (Gabrovska-Johnson et al. 2003), attention (Kucharska-Pietura et al. 2002), and ability to grasp global forms (Fermanetal. 1999).

The basic initial symptoms of schizophrenia not responsible to the modern neuroleptics (peculiarity of nonverbal behavior; deficiency of self-image; difficulty in grasping information to form a polydimensional picture of the complex situation and picture of the world; affective blunting; lack of empathy) can be explained by the inability to create and process the polysemantic context (Rotenberg 1994).

On the other hand, patients with dominating positive symptoms are characterized by the increased physiological and metabolic activity of the dysfunctional left hemisphere (Flor-Henry 1976; 1983; Friedman et al. 2001; Galderisi et al. 1999; Gur 1978; Gur & Chin 1999; Romney et al. 2000).

I have made an attempt to explain the relationship between the right and left hemisphere dysfunctions in schizophrenia (Rotenberg 1994). Integration with the world by means of the polysemantic way of thinking is the most important feature of a subjects mental health. Without such integration, the subject finds himself in front of a very complicated reality full of inner contradictions, and can use as an option an attempt to resolve difficult task by creating a simplified "left-hemispheric" model of reality. It does not fit. And then, in subjects predisposed to schizophrenic disorders, the left hemisphere creates an artificial explanatory system, in the form of delusions, paranoid ideas, and verbal hallucinations.

According to this proposition, functional right hemisphere deficiency is not unique to schizophrenia. Depression is characterized bv disrupted functional connections between anterior cinsu-late cortex and right orbitofrontal and prefrontal cortex regions (Pizzagalli et al. 2003) - very similar to what Burns suggest for the mechanism of schizophrenia. This means that the next problem we have to solve is what brain (and genetic) mechanisms predispose a subject who suffers from right hemisphere insufficiency to the development of the concrete forms of mental disorders. In the case of schizophrenia, what is it, for example, about the dopamin-ergic system that leads to a greater release of dopamine? (Zipursky & Kapur 1998).