Fear Conditioning following Unilateral Temporal Lobectomy: Dissociation of Conditioned Startle Potentiation and Autonomic Learning

Abstract

The present study investigated fear-potentiated startle and autonomic learning in brain-lesioned patients in a classical fear-conditioning paradigm. Startle blink and skin conductance responses of 30 patients who underwent unilateral temporal lobectomy because of drugresistant epilepsy were compared with those of 32 healthy controls. As expected, temporal lobectomy patients showed a general impairment in fear conditioning relative to controls. This impairment did not differ with respect to the affected hemisphere. Moreover, while fear-conditioned startle potentiation in healthy controls was independent of contingency awareness, skin conductance discrimination was only observed for those participants who correctly recognized the stimulus contingencies. Patients who acquired a declarative memory of the contingencies also showed intact skin conductance discrimination but failed to exhibit fear-potentiated startle. The present findings support a two-levels-of-learning account of human fear conditioning and also demonstrate that the amygdala is crucially involved in fear learning.

Role of corticotropin releasing factor in anxiety disorders: A translational research perspective

“…Responses to tactile (e.g., an airpuff to the throat or face) or acoustic stimuli are recorded in animals as a whole body "flinch response" and in humans as the strength of the eye blink response (EMG electrodes at the orbicularis oculi muscles). Cortical and limbic brain regions, many of which are abnormally activated or exhibit altered volumes in anxiety disorders (as measured by fMRI or PET e.g., Gilbertson et al, 2002;Hull, 2002;Lorberbaum et al, 2004;Neumeister et al, 2004;Schneider et al, 1999), modulate startle responses (Davis, 1998;Funayama et al, 2001;Kumari et al, 2003;Swerdlow et al, 2001;Weike et al, 2005). The magnitude of the response is highly plastic: fear-inducing stimuli (termed fear-potentiated startle; FPS) or administration of anxiogenic compounds, such as CRF, increases startle (Brown et al, 1951;Davis et al, 1997;Swerdlow et al, 1986), while threat-reducing stimuli (Lang et al, 1990), anxiolytic and sedative drugs (Abduljawad et al, 2001) or sensory input in the case of prepulse inhibition (PPI) Geyer et al, 2001;Graham, 1975;Swerdlow et al, 2001) reduces startle.…”

Increased stathmin expression strengthens fear conditioning in epileptic rats

“…Numerous patients reported the emotion of fear prior to seizures (2). Mesial temporal lobe epilepsy is commonly associated with ictal fear (3), and temporal lobectomy patients showed a general impairment in fear conditioning (4,5). However, the association between seizure-modulated fear and the underlying basics of neuronal mechanisms remains unclear.…”

Posttraumatic stress disorder in a patient with no left amygdala.

“…For instance, Baker and Kim (2004) observed that in rats, posttraining lesions to the right amygdala lead to a considerably larger impairment in (Buchanan, Tranel, & Adolphs, 2006). Damage to the right amygdala also has been observed to produce a more global deficit in electrodermal responses than damage to the left amygdala (Gläscher & Adolphs, 2003;Weike et al, 2005), perhaps reflecting an asymmetry in global autonomic control.…”

“…For instance, Baker and Kim (2004) observed that in rats, posttraining lesions to the right amygdala lead to a considerably larger impairment in (Buchanan, Tranel, & Adolphs, 2006). Damage to the right amygdala also has been observed to produce a more global deficit in electrodermal responses than damage to the left amygdala (Gläscher & Adolphs, 2003;Weike et al, 2005), perhaps reflecting an asymmetry in global autonomic control.Neuroimaging data have also pointed to functional asymmetries in amygdalar function. Several studies suggest that the right amygdala responds more to experientially learned or conditioned fearful stimuli, whereas, the left amygdala appears more active during the perception of innately fear-related items such as photographs of threatening stimuli or fearful faces (e.g., Büchel et al, 1998;Dolan and Morris, 2000;Morris et al, 1996Morris et al, , 1998.…”

“…In humans, temporal lobectomy patients show asymmetries in their recall of unpleasant autobiographical memories, with patients with right temporal lobectomies showing a decreased ability to recall unpleasant emotional events, while left temporal lobectomy patients show normal levels of recall (Buchanan, Tranel, & Adolphs, 2006). Damage to the right amygdala also has been observed to produce a more global deficit in electrodermal responses than damage to the left amygdala (Gläscher & Adolphs, 2003;Weike et al, 2005), perhaps reflecting an asymmetry in global autonomic control.…”