Massed and Spaced Learning in Honeybees: The Role of CS, US, the Intertrial Interval, and the Test Interval

Abstract

Conditioning the proboscis extension reflex of harnessed honeybees (Apis mellifera) is used to study the effect temporal spacing between successive conditioning trials has on memory. Retention is monitored at two long-term intervals corresponding to early (1 and 2 d after conditioning) and late long-term memory (3 and 4 d). The acquisition level is varied by using different conditioned stimuli (odors, mechanical stimulation, and temperature increase at the antenna), varying strengths of the unconditioned stimulus (sucrose), and various numbers of conditioning trials. How learning trials are spaced is the dominant factor both for acquisition and retention, and although longer intertrial intervals lead to better acquisition and higher retention, the level of acquisition per se does not determine the spacing effect on retention. Rather, spaced conditioning leads to higher memory consolidation both during acquisition and later, between the early and long-term memory phases. These consolidation processes can be selectively inhibited by blocking protein synthesis during acquisition.Learning trials distributed over time lead to better memory than learning trials squeezed into short periods of time. Jost (1897), who elaborated on the original findings by Ebbinghaus (1885), was the first to formulate a theory supposing a contraintuitive, even perplexing interrelation between short-term forgetting and long-term strengthening of memory. In his words, "Given equal associative strength, the older the memory trace at the time of learning repetition, the less forgetting over the long term." The "paradox of spaced practice" (Björk and Allen 1970) was assumed to lie in the fact that longer intervals between learning trials should lead to less memory on a trial-to-trial basis, but multiple units of less memory should finally lead to stronger long-term memory.The conceptual basis for interpreting the spacing effect is the notion of memory dynamics (James 1890; Müller and Pilzecker 1900;Squire 1987). Each learning trial is thought to initiate an intrinsic process of memory formation that leads to final memory by constructive (memory consolidation) and destructive (forgetting) processes. Studies of many species have shown that when training involves multiple trials, the time interval between trials is an important variable in the efficacy of accumulating training effects and the strength of retention (Carew et al. 1972;Fanselow and Tighe 1988;Tully et al. 1994;Spieler and Balota 1996;Kogan et al. 1997;Hermitte et al. 1999;Muzzio et al. 1999;Beck et al. 2000;Wu et al. 2001). The paradigms tested were taste aversion conditioning, fear conditioning, blink conditioning, olfactory aversion training, episodic priming, and learning nonsense syllables. In addition to humans, a wide range of animals was studied (Drosophila, the marine mollusks Aplysia and Hermissenda, the crab Chasmagnathus, rats, and rabbits). The dynamics and interdependence of the constructive and destructive (forgetting) memory processes, and, particularly, their relianc...

Role of Cerebellar Cortical Protein Synthesis in Transfer of Memory Trace of Cerebellum-Dependent Motor Learning

“…In rabbit eyeblink conditioning, infusions of anisomycin into the cerebellar interpositus nuclei depress both the acquisition and retention of the conditioned response (Bracha et al, 1998;Gomi et al, 1999). The role of protein synthesis has been suggested in the memory acquisition induced by the spaced training in the conditioning of the proboscis extension reflex of honey bees (Menzel et al, 2001) and in the contextual learning of fear conditioning in rats (Scharf et al, 2002).…”

Interaction between Amount and Pattern of Training in the Induction of Intermediate- and Long-Term Memory for Sensitization in Aplysia

“…For example, Sutton et al (2001b) have recently identified a second (activity-dependent) form of memory for sensitization in Aplysia that is expressed in the same temporal domain as L-ITM described in the present paper (see also, Sutton et al 2001a); however, unlike the form of L-ITM examined in the present study, this form of sensitization does not require protein synthesis. In addition, Menzel et al (2001) have recently shown that 1-2 d memory for conditioning of the proboscis extension reflex in honeybees after spaced training is significantly diminished by protein synthesis inhibitors, whereas 1-2 d memory after massed training is not. Thus, whereas different temporal phases of memory may have distinct mechanisms, time alone is not sufficient to characterize the properties of memory existing in a given temporal domain.…”

“…In particular, in a variety of tasks across species ranging from invertebrates to humans, training trials distributed over time (spaced training) typically lead to superior retention compared with training in which trials are presented with little or no rest interval (massed training) (Ebbinghaus 1885;Carew et al 1972;Salafia et al 1973;Lefebvre and Sabourin 1977;Fanselow and Tighe 1988;Tully et al 1994;Hermitte et al 1999;Muzzio et al 1999;Menzel et al 2001). Perhaps the most interesting feature of the superiority of spaced over massed training is that it is not a general effect for all temporal domains of memory but rather appears to become more pronounced with longer-lasting memories (e.g., Carew et al 1972;Tully et al 1994;Menzel 2001). Thus, an understanding of the behavioral, cellular, and molecular factors contributing to the massed versus spaced effect could yield considerable insight into the overall organization of multiple phases of memory.…”

Behavioural Pharmacology in Classical Conditioning of the Proboscis Extension Response in Honeybees (<em>Apis mellifera</em>)

“…3. Olfactory conditioning: The number of conditioning trials, the inter-trial interval, and the test time point can be varied depending on the focus of the study 3,22 . 4.…”