E.J. Neafsey (1993) Frontal Cortex, the Mind, and the Body. Psycoloquy: 4(15) Frontal Cortex (2)

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PSYCOLOQUY (ISSN 1055-0143) is sponsored by the American Psychological Association (APA).
Psycoloquy 4(15): Frontal Cortex, the Mind, and the Body

FRONTAL CORTEX, THE MIND, AND THE BODY
Commentary on Abbruzzeze et al. on Frontal-Cortex

E.J. Neafsey
Department of Cell Biology, Neurobiology & Anatomy
Loyola University Medical Center
2160 S. First Avenue
Maywood, IL 60153 USA

KEYWORDS: cognitive disorder, dorsolateral prefrontal cortex,
mental disorder, neuropsychology, obsessive-compulsive disorder,
orbitofrontal cortex, psychosis, schizophrenia.

eneafsey@lucpug.it.luc.edu

Abstract

The fundamental problem with attempting to understand frontal cortical function using the computer-inspired, functionalist models of contemporary cognitive science is that such models are by definition "disembodied." As a result, the brain as well as the mind tends to become disembodied, even "ghostly," in the traditional, dualistic, Cartesian fashion, (Ryle [1949/1984] notwithstanding). Far better are attempts rooted in the views of Hughlings Jackson, for whom the brain from "bottom to top" never lost its fundamental and basic bodily orientation. Human beings think and know in an inescapably and inherently bodily manner, even at the "highest levels" of the prefrontal cortex. As Gleick (1992) notes in his biography of Richard Feynman, the physicist legendary for his intuitive understanding of the abstract and unimaginable theories of quantum mechanics, "Those who watched Feynman in moments of intense concentration came away with a strong, even disturbing sense of the physicality of the process, as though his brain did not stop with the gray matter but extended through every muscle in his body."

Keywords

cognitive disorder, dorsolateral prefrontal cortex, mental disorder, neuropsychology, obsessive-compulsive disorder, orbitofrontal cortex, psychosis, schizophrenia.

I. INTRODUCTION

1.1 In any discussion of frontal lobe function it is absolutely imperative to keep in mind the "motor outputs to the body" generated by the frontal lobe regions in question. Otherwise the discussion tends to leap quickly into abstract theories of higher cognitive function or descriptions of complex, self-contained cortico-cortical networks that appear utterly unconnected to the more mundane level of sensorimotor processing that describes what's really going on. Hughlings Jackson's (1887-88) assertion that the nervous system is "a sensori-motor mechanism from bottom to top; that every part of the nervous system represents impressions or movements, or both" applies most especially to the frontal lobe, precisely because it has so often been linked to "purely mental" higher cognitive activities. Irving Diamond (1979) expressed this Jacksonian view in another way when he argued that the "motor cortex" is best conceived not as restricted to the precentral gyrus but rather as layer V of the entire cerebral cortex. This is true because layer V, no matter where it is, contains neurons that project to subcortical "motor" targets such as the spinal cord, brainstem, or hypothalamus. (Diamond likewise argues that layer IV everywhere is the "sensory cortex" and that layers II and III everywhere are the "association cortex.")

1.2 For the target article (Abbruzzese et al., 1993), then, it is important to remember that the dorsolateral prefrontal cortex and the orbitofrontal cortex have descending motor outputs that provide important clues about their functions. The dorsolateral prefrontal cortex projects directly to the superior colliculus (Goldman and Nauta, 1976), a midbrain structure that has a prominent role in the control of eye and head movements (Sparks, 1991). The orbitofrontal cortex, in contrast, projects directly to brainstem and and spinal visceral motor structures related to the autonomic nervous system and is also an important olfactory and visceral sensory area (see review by Neafsey, 1990).

II. DORSOLATERAL PREFRONTAL CORTEX AND "LOOKING"

2.1 The target article attributed the excessive perseverative errors on the Wisconsin Card Sorting Test (WCST-PE) in schizophrenics to dorsolateral prefrontal cortex (DLPFC) damage or malfunction. I agree with Abbruzzeze et al. that the fundamental deficit following damage to this region is exactly this type of perseveration. The authors, however, do not attempt to "explain" why such perseverative errors occurred in either schizophrenics or following DLPFC damage. In contrast, another recent study of schizophrenics that also found perseverative deficits using a different task (oculomotor delayed response; Park and Holzman, 1992) went further and attributed the increased errors to impaired "spatial working memory," echoing Goldman-Rakic's (1987) interpretation of similar deficits on the same task in monkeys with DLPFC lesions. I have previously argued against such an interpretation, basing my objection on an extensive review of the prefrontal literature that hod found many studies explicitly rejecting a "memory hypothesis" (Neafsey, 1990). Instead, most studies strongly supported an "interference hypothesis" related to "excessive distractability."

2.2 This basic deficit was identified long ago by Malmo (1942), who originally proposed the "interference hypothesis" to explain frontal lobe delayed response deficits in monkeys. Pribram (1973) reaffirmed the viability of this hypothesis, asserting that it was "as it has been for three decades, the most viable and useful in explaining the effects of resection of the dorsolateral frontal cortex of primates." Evidence that the delayed response deficits in prefrontal primates are NOT memory deficits is provided by the COMPLETE RESTORATION of delayed response performance to normal levels in prefrontal animals by a variety of simple strategies that reduced "interfering" distractions or enhanced motivation. These included turning off the lights in the animal chamber during the delay (Malmo, 1942), delivering an additional food reward at stimulus presentation before delay begins (Finan, 1942), lightly sedating the monkeys with Nembutal (Wade, 1947), making them hungrier or colder (Pribram, 1950), or running sham release trials with no reward to extinguish responses to release after the delay (dogs; Konorski and Lawicka, 1964).

2.3 This last experiment (Konorski's dogs) is most revealing. Dogs were held by their trainer in front of three feeding tables (left, center, right). A clicking sound emanated from the "correct" table. The clicking sound stopped, a delay ensued, and then the dog was released. If he went to the correct table, he was fed. After training, normal dogs performed this task easily, while prefrontal dogs made many perseverative errors (often going to the same table every time no matter where the clicking was). What is most illuminating, however, is what the prefrontal dogs did AFTER they initially went to the incorrect table. With a choice of two remaining tables to approach, they ALWAYS went to the correct table! This demonstrates a perfectly intact memory, thereby eliminating any spatial working memory deficit explanation.

2.4 Guitton et al. (1985; also see Butter et al., 1989) showed that unilateral DLPFC lesions in man impair SUPPRESSION of saccades to the contralateral side. These subjects could not inhibit looking at a target that appeared on the screen even though they knew the task required them to look away from it because the "real target" would subsequently appear on opposite side. Thus, a simple sensorimotor deficit (can't inhibit looks = distractability => interference) can have devastating "cognitive" effects. This sensorimotor concept of DLPFC function is consistent with the target article's description of how schizophrenics could not easily "shift" ("look away"?) to a new response set during the WCST.

III. ORBITOFRONTAL CORTEX AND "FEELING"

3.1 The target article attributes the excessive perseverative errors on the object alternation test (OAT) in subjects with obsessive compulsive disorder (OCD) to malfunction of the orbitofrontal cortex. In my opinion, any such explanation for these deficits must take into account several recent striking findings about the orbitofrontal cortex indicating that its primary role lies in the realm of affect and emotion.

3.2 The first important fact about the orbitofrontal cortex is that its primary motor output is directed at the autonomic and endocrine systems (see review by Neafsey, 1990). This includes DIRECT projections to brainstem and spinal autonomic "centers" such as the solitary nucleus of the vagus, periaqueductal gray, laterodorsal tegmental nucleus, and the sympathetic preganglionic neurons in the thoracic intermediolateral cell column (Terreberry and Neafsey, 1987; Hurley et al., 1991). These findings firmly plant the orbitofrontal cortex in the sensorimotor sphere.

3.3 The second and perhaps most important fact about the orbitofrontal cortex is that this is where EVR's primary brain damage is located. EVR is a patient who sustained bilateral damage to his orbitofrontal cortices during surgical removal of a brain tumor (Eslinger and Damasio, 1985). Despite intact and even above average or superior intelligence, memory, language, etc. following surgery, EVR was radically changed for the worse.

3.4 At the time of his operation EVR was a financial officer with a small company and a respected member of his community. He was married and the father of two children; his brothers and sisters considered him a role model and a natural leader. After the operation, EVR lost his job, went bankrupt, was divorced by his wife, and moved in with his parents. He subsequently married a prostitute and was divorced again within two years. Extensive psychological evaluations found no deficit; in fact, he was superior or above average on most tests (e.g., Verbal IQ of 125; Performance IQ of 124; normal MMPI; no difficulty on Wisconsin Card Sorting Test). He was also able to discuss the economy, foreign affairs, financial matters, and moral dilemmas sensibly and intelligently. Despite these normal findings, EVR was often unable to make simple, rapid decisions about what toothpaste to buy, what restaurant to go to, or what to wear. He would instead become stuck making endless comparisons and contrasts, often making no decision at all or a purely random one.

3.5 The clue that has led to a plausible explanation for EVR's puzzling combination of consistently poor decisions with superior cognitive abilities was the unexpected finding that he (and five other similar cases; Damasio et al., 1990) totally lacked sympathetically mediated skin conductance responses to both neutral and emotional visual images. A normal individual displays a much larger skin conductance response to a picture of a horribly mutilated automobile accident victim than he does to a picture of a table, for example. EVR's skin conductance recording was a flat line to both images -- no response at all, no distinction. In fact, at the end of the testing session EVR "noted that he had not experienced the kind of 'feeling' that he thought he ought to have in relation to some stimuli, given their content" (Damasio et al., 1990). (Interestingly, EVR did display skin conductance changes when he had to verbally describe the pictures as he viewed them.)

3.6 Luria and Homskaya (1964) had described similar frontal patients lacking skin conductance responses some years ago; Nauta (1971) insightfully termed their deficit "interoceptive agnosia" -- an ignorance due to the absence of normal visceral and somatic bodily responses that function as critical cues to the meaning or value of situations and thoughts. In other words, because EVR lacks normal physiological responses, he also lacks normal, immediate, intuitive, "gut feelings" to guide him through his decisions about either important or trivial matters. [This analysis recalls William James's so-called peripheral theory of the emotions (James, 1890); even critics of "peripheral" theories of emotion (e.g., Reisenzein, 1983) admit that physiological responses intensify emotional experience.] Damasio termed EVR's deficit "acquired sociopathy" because sociopaths also respond inappropriately to social situations and, interestingly, often show impaired or absent skin conductance responses (Damasio et al., 1990; Hare et al., 1978). My own laboratory (Frysztak and Neafsey, 1991) has reported similar reduced autonomic and behavioral fear responses in rats following frontal lesions.

3.7 A possible link between EVR and the OCD subjects studied in the target article is EVR's inability to make decisions because he became "stuck making endless comparisons and contrasts" as mentioned above. This is reminiscent of obsessive-compulsive behavior and suggests that an absence or diminution of normal emotion or feelings allows cognitive, "rational" evaluation to proceed endlessly because no "value" or "emotional preference" for one alternative can be established that stops the process. Perhaps the OCD subject cannot alternate because the "correct" choice lacks its normal emotional weight or force because it cannot be adequately "somatically marked" (Damasio et al., 1990) by normal amplitude physiological responses.

IV. CONCLUSION

4.1 The fundamental problem with attempting to understand frontal cortical function using the computer-inspired, functionalist models of contemporary cognitive science is that such models are by definition "disembodied." As a result, the brain as well as the mind tends to become disembodied, even "ghostly," in the traditional, dualistic, Cartesian fashion, (Ryle [1949/1984] notwithstanding). Far better are attempts rooted in the views of Hughlings Jackson, for whom the brain from "bottom to top" never lost its fundamental and basic bodily orientation. Human beings think and know in an inescapably and inherently bodily manner, even at the "highest levels" of the prefrontal cortex. As Gleick (1992) notes in his biography of Richard Feynman, the physicist legendary for his intuitive understanding of the abstract and unimaginable theories of quantum mechanics, "Those who watched Feynman in moments of intense concentration came away with a strong, even disturbing sense of the physicality of the process, as though his brain did not stop with the gray matter but extended through every muscle in his body."

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