Role of the hippocampus in contextual memory after classical aversive conditioning in pigeons (C. livia)

Abstract

We investigated the effects of hippocampal lesions with ibotenic acid (IBO) on the memory of the sound-context-shock association during reexposure to the conditioning context. Twenty-nine adult pigeons were assigned to a non-lesioned control group (CG, N = 7), a shamlesioned group (SG, N = 7), a hippocampus-lesioned experimental group (EG, N = 7), and to an unpaired nonlesioned group (tone-alone exposure) (NG, N = 8). All pigeons were submitted to a 20-min session in the conditioning chamber with three associations of sound (1000 Hz, 85 dB, 1 s) and shock (10 mA, 1 s). Experimental and sham lesions were performed 24 h later (EG and SG) when EG birds received three bilateral injections (anteroposterior (A), 4.5, 5.25 and 7.0) of IBO (1 µl and 1 µg/µl) and SG received one bilateral injection (A, 5.25) of PBS. The animals were reexposed to the training context 5 days after the lesion. Behavior was videotaped for 20 min and analyzed at 30-s intervals. A significantly higher percent rating of immobility was observed for CG (median, 95.1; range, 79.2 to 100.0) and SG (median, 90.0; range, 69.6 to 95.0) compared to EG (median, 11.62; range, 3.83 to 50.1) and NG (median, 7.33; range,6.2 to 28.1) (P<0.001) in the training context. These results suggest impairment of contextual fear in birds who received lesions one day after conditioning and a role for the hippocampus in the modulation of emotional aversive memories in pigeons.

Classical tone-shock conditioning induces zenk expression in the pigeon (Columba livia) hippocampus.

“…These results are primarily important as indicative of molecular mechanisms that are triggered in the hippocampus of pigeons during the acquisition of conditioned fear. In this context, they corroborate experimental evidence from lesion studies and are thus consistent with studies in birds and in mammals that indicate the striking functional importance of the hippocampus in fear conditioning (Bast et al, 2001, 2003; Kim & Fanselow, 1992; Reis et al, 1999).…”

“…The widely accepted assumption that the hippocampus plays an essential role in learning and memory is supported by information on primates (Akhondzadeh, 1999; Eichenbaum, Otto, & Cohen, 1992; Martin, Grimwood, & Morris, 2000; Shiflett, Smulders, Benedict, & De Voogd, 2003) and rodents (Guzowski, Setlow, Wagner, & McGaugh, 2001; Sprick, 1995; Tischmeyer & Grimm, 1999), as well as data on the avian hippocampus (Colombo & Broadbent, 2000; Reis, Schenka, Mello, & Ferrari, 1999; Watanabe, 2000). These studies emphasize that the hippocampus plays a crucial role in behavioral regulation and cognition, especially spatial, contextual, and relational types of learning (Abel & Lattal, 2001; Antoniadis & McDonald, 2000; Eichenbaum et al, 1992; Kim & Fanselow, 1992; Silva, Giese, Fedorov, Frankland, & Kogan, 1998).…”

The Importance of Hippocampus-Dependent Non-Spatial Tasks in Analyses of Homology and Homoplasy

“…Rats (R. norvegicus) with HP lesions are impaired in incidental [Good and Honey, 1991;Good et al, 1998] and conditioned [Benoit et al, 1999] learning of context. HP-lesioned pigeons (C. livia) are impaired in contextual fear conditioning [Reis et al, 1999].…”

Aversive conditioning in the tardigrade, Dactylobiotus dispar.

“…Parallels have been made between the neural circuits supporting aversive conditioning and extinction in rodents and humans in attempts to better understand the biological bases of this defensive behavior (Delgado, Olsson, & Phelps, 2006). Moreover, aversive conditioning has been demonstrated in other mammals, including dogs (Moscovitch & LoLordo, 1968; Rescorla, 1968), cats (Diamond & Weinberger, 1984; Ryugo & Weinberger, 1978), rabbits (Jarrell, Gentile, Romanski, McCabe, & Schneiderman, 1987; Supple & Kapp, 1989), and nonhuman primates (Cook & Mineka, 1989; Melamed, Jesus, Maior, & Barros, 2017), and other vertebrates, such as birds (Jarvis, Mello, & Nottebohm, 1995; Maser, Gallup, & Barnhill, 1973; Reis, Schenka, Melo, & Ferrari, 1999) and fish (Barela, 2015; Kenney, Scott, Josselyn, & Frankland, 2017)—all likely having similar circuits that support aversive conditioning. Useful information has been gained from this approach, perhaps most important being the development and refinement of exposure therapies to treat anxiety disorders in humans (Ganella, Drummond, Ganella, Whittle, & Kim, 2018; Mears & Pollard, 2016; Mineka & Oehlberg, 2008; Vanelzakker, Dahlgren, Davis, Dubois, & Shin, 2014).…”