The amygdala is critical for trace, delay, and contextual fear conditioning

Abstract

Numerous investigations have definitively shown amygdalar involvement in delay and contextual fear conditioning. However, much less is known about amygdala contributions to trace fear conditioning, and what little evidence exists is conflicting as noted in previous studies. This discrepancy may result from selective targeting of individual nuclei within the amygdala. The present experiments further examine the contributions of amygdalar subnuclei to trace, delay, and contextual fear conditioning. Rats were trained using a 10-trial trace, delay, or unpaired fear conditioning procedure. Pretraining lesions targeting the entire basolateral amygdala (BLA) resulted in a deficit in trace, delay, and contextual fear conditioning. Immediate post-training infusions of the protein synthesis inhibitor, cycloheximide, targeting the basal nucleus of the amygdala (BA) attenuated trace and contextual fear memory expression, but had no effect on delay fear conditioning. However, infusions targeting the lateral nucleus of the amygdala (LA) immediately following conditioning attenuated contextual fear memory expression, but had no effect on delay or trace fear conditioning. In follow-up experiments, rats were trained using a three-trial delay conditioning procedure. Immediate post-training infusions targeting the LA produced deficits in both delay tone and context fear, while infusions targeting the BA produced deficits in context but not delay tone fear. These data fully support a role for the BLA in trace, delay, and contextual fear memories. Specifically, these data suggest that the BA may be more critical for trace fear conditioning, whereas the LA may be more critical for delay fear memories.

Figure 1.

(A) Timeline for Experiment 1. (B) The minimum (black) and maximum (gray) extent of bilateral lesions in BLA (atlas images taken and modified from Paxinos and Watson 1998 with permission from Elsevier 1998). The number of animals in each group was as follows: trace sham, n = 7; trace lesion, n = 7; delay sham, n = 8; delay lesion, n = 9; N = 31. (C) The percentage of time spent freezing during the baseline period (first 3 min), tone, and trace interval or trace interval equivalent during the tone test. (D) Simultaneously learned contextual fear expressed during the context test.

Figure 2.

(A) Timeline for Experiment 2. (B) Cannula placement for all animals included in Experiment 2 (atlas images taken and modified from Paxinos and Watson 1998 with permission from Elsevier 1998). The number of animals in each group was as follows: unpaired veh, n = 9, trace veh, n = 11; trace cyclo, n = 11; delay veh, n = 10; delay cyclo, n = 10; N = 51. (C) The percentage of time spent freezing during baseline period (first 3 min), tone, and trace interval or trace interval equivalent during the tone test. (D) Simultaneously learned contextual fear expressed during the context test.

Figure 3.

(A) Timeline for Experiment 3. (B) Cannula placement for all animals included in Experiment 3 (atlas images taken and modified from Paxinos and Watson 1998 with permission from Elsevier 1998). The number of animals in each group was as follows: trace veh, n = 8; trace cyclo, n = 8; delay veh, n = 9; delay cyclo, n = 10; N = 35. (C) The percentage of time spent freezing during the baseline period (first 3 min), tone, and trace interval or trace interval equivalent during the tone test. (D) Simultaneously learned contextual fear expressed during the context test.

Figure 4.

(A) Timeline for Experiment 4. (B) Cannula placement for all animals included in Experiment 4 (atlas images taken and modified from Paxinos and Watson 1998 with permission from Elsevier 1998). The number of animals in each group was as follows: delay veh, n = 11; delay cyclo, n = 11; N = 22. (C) The percentage of time spent freezing during the baseline period (first 3 min), tone, and context.

Figure 5.

(A) Timeline for Experiment 5. (B) Cannula placement for all animals included in Experiment 5 (atlas images taken and modified from Paxinos and Watson 1998 with permission from Elsevier 1998). The number of animals in each group was as follows: delay veh, n = 10; delay cyclo, n = 10; N = 20. (C) The percentage of time spent freezing during the baseline period (first 3 min), tone, and context.