Effects of prediction error and acute stress on retrieval-extinction of fear memories of different strengths

doi:10.3724/SP.J.1041.2021.00587

Abstract

Abstract:

Under the framework of Reconsolidation Interference of conditioned fear memory, Prediction Error (PE) has been demonstrated as a necessary condition of memory destabilization. However, the role of PE in destabilizing fear memories of different strengths is unclear. Memory strength was proved to be an important boundary condition of memory reconsolidation; however, explorations of solutions to overcome the boundary are rare. Among factors that are possible to help to overcome the boundary condition, the effects of stress hormones are worth exploring. In this study, we investigated the effects of prediction error on different strengths of fear memory in human participants and the effects of post-reactivation acute stress on the extinction process. The results showed that for weak conditioned fear memories, the spontaneous recovery of fear was significantly inhibited when single PE was involved in the retrieval phase; while for stronger fear memories, reactivation containing a single PE could not destabilize fear memories, and the extinguished memories returned in the memory test on the third day. Furthermore, when the post-reactivation acute stress task was adopted in the enhanced memory condition, the return of fear further increased, compared with the no stress manipulation conditions.

Key words: conditioned fear, retrieval-extinction, prediction error, acute stress, memory strength

LI Junjiao, CHEN Wei, HU Yanjian, CAOYANG Jingwen, ZHENG Xifu. (2021). Effects of prediction error and acute stress on retrieval-extinction of fear memories of different strengths. Acta Psychologica Sinica, 53(6), 587-602.

Figures/Tables 8

Table 1 Experimental grouping and sample size

Variable	Group			p
Variable	G1	G2	G3	p
Retrieval phase	Single PE	Single PE + SECPT	Single PE
N (SCR)	16	19	15
N (FPS)	15	21	23
Age	20.88 ± 1.54	20.04 ± 1.80	21.44 ± 2.58	0.069
STAI-T	37.35 ± 10.88	41.83 ± 7.10	39.78 ± 7.92	0.266
BDI	6.94 ± 4.53	8.44 ± 5.96	7.26 ± 5.83	0.655

Figure 1. Schema of the experimental procedure. A: the overall experimental procedure; B: the schema of the manipulation of the memory strength in the acquisition and the operation during reactivation.
Note. The manipulation of memory strength: on day 1, two shocks (US) appeared at unpredictable time points during the second half of the CS presentation; and the CS-unpredictable US association was expected to produce stronger fear memories (G1, G2). Using the two US at the fixed point of CS presentation time (4800 ms and 5800 ms, respectively), the CS-predictable US association was expected to produce a weaker fear memory (G3). The manipulation of prediction error (PE): on the next day, a trial of CS pared with a US on fixed time point (5800 ms) for all groups was used as reminders to retrieval memories; and the prediction error was induced by different number of shocks between the acquisition and retrieval period. Because all participants were given two shocks at the learning stage, the expectation was that each CS will follow US twice. But in the retrieval phase, CS was paired with US only once, resulting in a single prediction error (single PE).

Figure 2. Testing time points of each physiological index and questionnaire survey on day 1 and 2.
Note. Hab: habituation; Acq: acquisition; Ret: retrieval; Ext: extinction; WWT: warm-water task; BDI: Beck Depression Inventory; STAI-T: Trait Anxiety Inventory; PANAS: positive and negative emotion scale; BP: blood pressure; HR: heart rate; SF: subjective perception; the number after each name represents the testing sequence of the test.

Figure 3. Comparison of low frequency components of heart rate variability in each group during SECPT.

Table 2 The frequency domain of heart rate variability (HRV) in each group on different timepoints of SECEPT or WWT

Experimental grouping	G1 n = 15	G2 n = 20	G3 n = 22	F	p
LF
before (pre)	71.70 ± 40.66	128.85 ± 108.95	120.87 ± 126.45	1.46	0.24
during (mid)	106.56 ± 145.84	227.76 ± 313.37	84.53 ± 82.59	2.29	0.11
after (post)	125.57 ± 109.65	130.52 ± 168.65	149.50 ± 181.47	0.12	0.89
HF
before (pre)	44.83 ± 38.65	96.02 ± 86.74	68.66 ± 65.67	2.43	0.10
during (mid)	73.57 ± 78.74	102.51 ± 100.09	74.11 ± 55.91	0.51	0.61
After (post)	55.46 ± 28.64	63.04 ± 40.96	88.76 ± 64.18	0.12	0.89

Figure 4. Three groups of participants in the fear memory acquisition, retrieval, extinction and testing of SCR.
Note. The x axis represents the trials: 1~6 for the first day of acquisition, 8 for the second day of retrieval, 10~19 for the second day of extinction, 21~28 for the third day of spontaneous recovery, and 30~37 for the third day of reinstatement. Error bar stands for standard error, and the electric shock is depicted as the yellow lightning symbol. (same in Figure 6)

Figure 5. The comparison of spontaneous recovery and reinstatement of fear in each group. A: Results on SCR; B: results on FPS.
Note. The amount of spontaneous recovery of fear = the first CS+ fear response of re-extinction - the last CS+ fear response of extinction; The amount of fear reinstatement = the first CS+ fear response of the final extinction - the last CS+ fear response of re-extinction. * p <0.05, ** p <0.01.

Figure 6. Three groups of participants’ startle response in fear memory acquisition, retrieval, extinction and tests.

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