Stewart H. Hulse

Structural complexity as a determinant of serial pattern learning

Abstract A new methodology extends the study of serial pattern learning to nonhuman organisms by constructing patterns using elements that are both familiar and motivationally meaningful to animals. Two experiments examine the ability of rats to anticipate various quantities of food as measured by running times in a runway when the quantities occur in a serial order. In Experiment 1, a serial monotonic pattern (14-7-3-1-0 food pellets) produced more rapid learning and more accurate anticipation of the various quantities (“tracking”) than a serial nonmonotonic pattern (14-1-3-7-0 food pellets), particularly with respect to the final 0-pellet element. In Experiment 2, the same monotonic pattern generated faster learning and more accurate anticipation of pattern elements than a weakly monotonic pattern (14-5-5-1-0 pellets). Associative explanations including simple excitatory or inhibitory effects, temporal anticipation, reinforcement contrast, and the number and discriminability of pairwise associations are not adequate to account for the data. Rather, the formally defined structural complexity of each pattern adequately predicts its relative difficulty.

Serial pattern learning by rats: Transfer of a formally defined stimulus relationship and the significance of nonreinforcement

Two experiments with rats tested independent predictions from cognitive theories of serial pattern learning. The animals learned to anticipate, as measured by running times in a straight alley, different quantities of food pellets organized into formally defined, five-element serial patterns. In Experiment 1, for some animals the patterns were all formally structured according to a monotonic “less than” relationship in which any quantity was always less than its predecessor. For others, no consistent formal rule was applied. Results of a transfer test with a new pattern showed positive transfer if the formal structure of the new pattern was identical to that used initially, but negative transfer if the new pattern was formally different. In Experiment 2, two groups learned the monotonic patterns 18-10-6-3-1 or 18-10-6-3-0 food pellets, while two others learned the nonmonotonic patterns 18-3-6-10-1 or 10-3-6-10-0 food pellets. We asked if the difference in value of the terminal element, 1 or 0 food pellets, would affect the facility with which the patterns were learned. The results showed that learning rate and the qualitative response to the elements of the monotonie and nonmonotonic patterns were independent of the value of the terminal element. Both experiments lend additional support to the utility of using cognitive models of human serial-pattern learning for an analysis of the sequential behavior of nonhuman animals.

Response biases in auditory forebrain regions of female songbirds following exposure to sexually relevant variation in male song

In many species of songbirds, individual variation between the songs of competing males is correlated with female behavioral preferences. The neural mechanisms of song based female preference in songbirds are not known. Working with female European starlings (Sturnus vulgaris), we used immunocytochemistry for ZENK protein to localize forebrain regions that respond to sexually relevant variation in conspecific male song. The number of ZENK-ir cells in ventral caudo-medial neostriatum [NCMv] was significantly higher in females exposed to longer songs than in those exposed to shorter songs, whereas variation in the total duration of song exposure yielded no significant differences in ZENK expression. ZENK expression in caudo-medial ventral hyperstriatum [cmHV] was uniformly high in all subjects, and did not vary significantly among the three groups. These results suggest that subregions of NCM in female starlings are tuned to variation in male song length, or to song features correlated therewith. Female starlings exhibit robust behavioral preferences for longer over shorter male songs (Gentner and Hulse; Anim Behav 59:443-458, 2000). Therefore, the results of this study strongly implicate NCM in at least a portion of the perceptual processes underlying the complex natural behavior of female choice.

Female European starling preference and choice for variation in conspecific male song

Data from several field studies support the hypothesis that female European starlings, Sturnus vulgaris, attend to variation among the songs of conspecific males when making mate-choice decisions. However, for a variety of methodological reasons, direct evidence for female preferences based on song in starlings has been lacking. This study presents a novel technique for assaying directly female preference and choice in European starlings by using the presentation of conspecific male song as an operant reinforcer in a controlled environment. Using an apparatus in which the playback of songs from different nestboxes is under the operant control of the subject, we demonstrate how the reinforcing properties of conspecific song can be used to measure female preference and choice. The results of the study suggest three conclusions. First, female starlings prefer naturally ordered conspecific male songs over reversed songs. Second, female starlings display robust preferences for longer compared with shorter male song bouts. Behaviour in the operant apparatus varied directly with male song bout length. Third, preferences based on song bout length are sex specific. Male starlings failed to respond differentially to the same stimuli for which females showed strong preferences. These results suggest that male-male variation in song bout length is important for mate choice among starlings. In addition, we detail the use of a novel behavioural assay for measuring female preferences that can be applied to similar behaviours in other species of songbirds. Copyright 2000 The Association for the Study of Animal Behaviour.

Auditory scene analysis by songbirds: stream segregation of birdsong by European starlings (Sturnus vulgaris).

Three experiments examined the capacity of European starlings to segregate perceptually 2 superimposed, intermixed auditory stimuli. The stimuli were 10-s song samples from 2 of 4 songbird species: European starling, brown thrasher, mockingbird, and nightingale. The birds first learned a discrimination between the intermixed song pairs. Then, they maintained the discrimination with novel song exemplars in the mixtures and when song stimuli for each species were presented alone. Performance fell, but remained above chance, when song pairs were mixed with the dawn chorus of bird song. The results show that starlings were identifying the songs of individual species within the baseline superimposed song pairs, a process of auditory stream segregation and scene analysis (A. S. Bregman, 1990).

Perceptual mechanisms for individual vocal recognition in European starlings,Sturnus vulgaris

The capacity for vocal recognition of individual conspecifics is well documented in many species, but the perceptual mechanisms that underlie this ability in oscines are less well understood. Using operant conditioning, we trained three groups of European starlings on a baseline task to discriminate the songs of one male starling from those of four others. Each subject heard songs from the same five singers, but the to-be-recognized individual varied among birds. We grouped the subjects according to sex and their degree of previous exposure to the songs used as stimuli in this experiment. The first group (N=5 males) identified their own songs from those of four familiar males. The second group (N=5 males) was familiar with the song stimuli, but none of the songs was their own. The third group (N=4 females) was unfamiliar with the songs. After learning the baseline discrimination, the subjects were exposed to new natural and synthetic stimuli. The subjects maintained the ability to identify correctly an individual on the basis of novel song bouts, and showed differential responding on the basis of the sequence of song types in song bouts that were modelled using Markov chains. Based upon patterns of responding to these different stimuli, we conclude that European starlings are capable of individual vocal recognition, and that this process is mediated by mechanisms involving the memorization of individually specific song types, the sequential ordering of song types within different bouts of an individual, and perhaps by individually specific spectral (or voice) characteristics that generalize across song types. Copyright 1998 The Association for the Study of Animal Behaviour.

Individual vocal recognition and the effect of partial lesions to HVc on discrimination, learning, and categorization of conspecific song in adult songbirds.

Among songbirds, the capacity to associate particular songs with particular singers (i.e., vocal recognition) forms the cognitive basis for more complex communication behaviors such as female choice and territoriality. In the present study, we combine operant conditioning techniques and excitotoxic lesions to the forebrain nucleus HVc to examine the role of this region in the discrimination, associative learning, and categorization of conspecific song. We trained adult male and female European starlings, Sturnus vulgaris, to recognize simultaneously the songs of several conspecific males. Then, using a series of transfer procedures, we demonstrate that correct recognition does not generalize to song bouts containing novel motifs from familiar singers. This suggests that starlings do not make use of individually invariant source or filter characteristics for vocal recognition. We then lesioned a portion of HVc bilaterally with ibotenic acid, and exposed the birds to a series of manipulations testing the discrimination, associative learning, and categorization of conspecific song. The lesions attenuated song production among males, but retention of the basic recognition task (i.e., maintenance of the discrimination) was unaffected. However, when the response contingencies were reversed-as a test of associative learning independent of discrimination-the initial performance and subsequent learning rate were negatively correlated with the size of the HVc lesions. This suggests that HVc plays a role in the formation of associations between a song and some referent. The results of this study are discussed in light of earlier claims regarding the role of HVc in the perceptual processing of conspecific song.

Neural bases of song preferences in female zebra finches (Taeniopygia guttata)

WE examined the neural bases of song preferences in female zebra finches Taeniopygia guttat a). Females performed more courtship displays in response to conspecific songs than to heterospecific songs. Following electrolytic lesion to the HVc (sometimes referred to as high vocal center), females maintained normal song preferences. However, following lesion to cHV (caudal hyperstriatum ventrale, an auditory area) females performed courtship displays at high rates in response to both conspecific and heterospecific song. Thus cHV, but not HVc, must be intact for female zebra finches to exhibit normal song preferences. Differences between this study and those showing HVc lesions disrupting song preferences in female canaries Serinus canari a indicate interspecific variation in the function of HVc in female songbirds.

Auditory scene analysis by European starlings (Sturnus vulgaris): Perceptual segregation of tone sequences

Like humans, animals that use acoustic stimuli to perceive their world ought to be able to parse the auditory scene into functionally significant sounds. The ability to do so ought to have significant adaptive value when, for example, an animal can identify the sounds of a predator among other natural noises. In earlier work it was shown that a species of songbird, the European starling, can identify excerpts of both its own song and songs from other avian species when the songs are mixed concurrently with other natural signals. In this experiment it is demonstrated that starlings can segregate two synthetic pure-tone sequences when the sequences differ in frequency. Taken together, the experiments show that at least one nonhuman species is capable of auditory scene analysis both for natural and for non-natural acoustic stimuli. This suggests in turn that auditory scene analysis may be a general perceptual process that occurs in many species that make use of acoustic information.

Extrapolation of serial stimulus patterns by rats

This experiment determined if rats could extrapolate a familiar serial sequence of diminishing food quantities by accurately anticipating a novel quantity added to the end of the sequence. In 13 days of training, rats ran in a straight runway to obtain quantities of food pellets presented in sequential order. A strongly monotonic group received repetitions of a formally simple pattern of 14-7-3-1 pellets of food, while weakly monotonic and nonmonotonic groups received formally more complex 14-5-5-1 and 14-3-7-1 patterns, respectively. In subsequent transfer, a 0-pellet quantity was added to each pattern, thus extending pattern length to five elements. Results of the very first pattern repetition containing the added 0-pellet element indicated that rats in the strongly monotonic condition, but not in the others, anticipated the reduced quantity before actually experiencing it. This result supports a cognitive, rule-learning hypothesis for serial learning by rats.