Mesial cortical lesions and fear behavior in the wild rat

Abstract

Defensive behaviors of wild Rattus rattus were examined following lesions of anterior or posterior mesial cortex or control lesions in lateral cortical areas. The experimental lesions did not reduce flight, fear-based biting, or reactivity to contact or handling in these wild rats. The high levels offear-related behaviors seen before surgery continued for all groups. Damage to the mesial cortex, which involves equivalents to the human prefrontal cortex, thus produced no indication of reductions in a variety of fear-related behaviors.In one of the most influential experiments in neurobiology to date, Fulton and Jacobsen (1935) found an indication of decreased reaction to frustration in one of two chimpanzees with presumably identical lesions of the frontal lobes. This experiment triggered not only experiments on relations of the frontal lobes and emotions, but also a neurosurgical discipline presently known as "psychosurgery" (Freeman & Watts, 1942;Moniz, 1936). Today, "the most appropriate candidates for psychosurgery are patients described as suffering from very intense and persistent emotional responses" (Valenstein, 1980b, p. 89). The mesial frontal cortex is a frequent target of neurosurgeons for relief from these symptoms (Valenstein, 1980a).The role of the prefrontal cortex in "emotionality" is controversial: some experiments suggest such an involvement (Butter & Snyder, 1972;Kolb, 1974;Markowska & Lukaszewska, 1980), whereas others do not (e.g., Ursin & Divac, 1975). This controversy, which may be explained by differences in the studied species, the ablated cortical area, and the applied tests (Ursin & Divac, 1975) is not found when other properties of the prefrontal cortex are considered. Thus, in all studied species, the prefrontal area, defined as the cortical target of the thalamic mediodorsal nucleus, was found to receive a strong dopaminergic innervation (e.g., Divac, Bjorklund, Lindvall, & Passingham, 1978) and to mediate delayed response-type behavior (e.g., Wikmark, Divac, & Weiss, 1973).Relevance for psychosurgery requires detailed knowledge of the consequences of prefrontal lesions on var- ious aspects of emotional behavior. In the present study, we used wild trapped rats (Rattus rattus), which show more complete species-specific emotional behavior than do laboratory strains (Takahashi & R. J. Blanchard, 1982). In our animals, either the anterior or posterior mesial cortex was ablated. This part of the rat cortex has been considered to be especially involved in speciesspecific behaviors (Thomas, Hostetter, & Barker, 1968) and its rostral half in some aspects of emotional behavior (Kolb, 1974;Markowska, & Lukaszewska, 1980). Anatomically, the rat anterior mesial cortex contains equivalents of the frontal eye field, the anterior limbic cortex, and both the medial and dorsolateral prefrontal cortex of the monkey (and presumably human) brain (see, e.g., Divac, Kosmal, Bjorklund, & Lindvall, 1978). METHODS AND PROCEDURES SurgeryThe lesions were made in rats anesthetized with pentobarbital by gentle ...

The Role of the Medial Prefrontal Cortex in the Conditioning and Extinction of Fear

“…One of the first studies to examine the role of mPFC in defensive behaviors showed that damage to this structure had no effect on flight, biting or reactivity to handling in wild rats, although these lesions primarily encompassed more dorsal regions than PL and IL (i.e., ACC; Divac et al, 1984 ). In contrast to this report, dmPFC lesions (encompassing ACC/dorsal PL) in laboratory rats increased reactivity to an aversive stimulus and it was shown that these animals were capable of maintaining long-term fear, suggesting that dmPFC is not necessary for memory formation and retention or fear expression (Holson, 1986 ).…”

Differential contribution of dorsal and ventral medial prefrontal cortex to the acquisition and extinction of conditioned fear in rats.

“…The prefrontal cortex contains a number of anatomically and functionally distinct subregions, one of which is the midline area, the medial prefrontal cortex (mPFC; see Kolb, 1990, for review). There is now strong evidence that mPFC is involved in emotional processes (Divac, Mogenson, Blanchard, & Blanchard, 1984; Frysztak & Neafsey, 1991; Holson, 1986; Kolb, 1974; Markowska & Lukaszewska, 1980), particularly in the aversive domain (Al Maskati & Zbrozyna, 1989). It is part of the circuitry involved in modulating cardiovascular (Powell, Watson, & Maxwell, 1994), dopamine (Thierry et al, 1994; Thierry, Tassin, Blanc, & Glowinski, 1976), and ACTH/corticosterone (Diorio, Viau, & Meaney, 1993) responsivity to aversive stimuli.…”

“…Behavioral studies have produced conflicting results concerning the function of mPFC in fear conditioning, with lesions giving rise to increases (Frysztak & Neafsey, 1994; Holson, 1986; Morgan, Coons, & LeDoux, 1993; Morgan, Romanski, & LeDoux, 1993), decreases (Frysztak & Neafsey, 1991), or no change (Divac et al, 1984) in fear reactivity. It is possible that the contradictory findings are related to the placement of lesions in different aspects of mPFC.…”

Early lesion of the reticular thalamic nucleus disrupts the structure and function of the mediodorsal thalamus and prefrontal cortex

“…However, despite the PFC's involvement in the regulation of emotion, its contribution to the development of this behavior remains largely debated (Frysztak & Neafsey, ; Holson & Walker, ; Morgan & LeDoux, ; Morgan, Romanski, & LeDoux, ). Thus, some authors have argued that PFC injury induces an exacerbation of anxious attitude (Holson & Walker, ; Morgan & LeDoux, ), while others have shown that anxiety levels expressed by animal do not depend on the integrity of the PFC (Divac, Mogensen, Blanchard, & Blanchard, ; Lacroix, Broersen, Weiner, & Feldon, ). Moreover, the study by Frysztak and Neafsey () showed that the aspiration of the medial part of the PFC has an anxiolytic effect and favors the exploration of the open arms of the raised labyrinth.…”