Conspecific song preference is the ability songbirds require to distinguish conspecific song from heterospecific song in order for females to choose an appropriate mate, and for juvenile males to choose an appropriate song tutor during vocal learning. Researchers studying the swamp sparrow (Melospiza georgiana) have demonstrated that young birds are born with this ability, because juvenile males raised in acoustic isolation and tutored with artificial recordings choose to learn only songs that contain their own species' syllables.Marler, P. and S. Peters. 1977. Selective vocal learning in a sparrow. Science 198:519-521. Studies conducted at later life stages indicate that conspecific song preference is further refined and strengthened throughout development as a function of social experience.Amin, N., A. Doupe, and F. Theunissen. 2007. Development of selectivity for natural sounds in the songbird auditory forebrain. Journal of Neurophysiology 97:3517. The selective response properties of neurons in the songbird auditory pathway has been proposed as the mechanism responsible for both the innate and acquired components of this preference.
Neural mechanisms The mechanism responsible for the ability to distinguish song types has not yet been fully characterized by researchers in the field of neuroethology, but it has been demonstrated that at least five different structures within the auditory pathway contain neurons that preferentially respond to conspecific song. The structure of neural networks, the morphology of neurons, and the receptor and ion channel complement of pre-synaptic connections cause some neurons to respond maximally to a particular stimulus frequency, phase, amplitude or temporal pattern, and this is known as spectral-temporal tuning.Woolley, A.M.N., T.E. Fremouw, A. Hsu and F.E. Theunissen. 2005. Tuning for spectro-temporal modulations as a mechanism for auditory discrimination of natural sounds. Nature Neuroscience 8:1371-1379. Tight spectral-temporal tuning in the auditory pathway provides the central nervous system of songbirds with the ability to discriminate between conspecific and heterospecific songs. Tuning characteristics of auditory neurons have been best characterized in zebra finch (Taeniopygia guttata), canary (Serinus canaria), European starling (Sturnus vulgaris) and Western barn owl (Tyto alba).
Learning and motor pathways The conventional song system of songbirds has two parts: the anterior forebrain pathway (AFP) involved in song learning, and the posterior forebrain pathway or "song motor pathway" (PFP/SMP) involved in song production. Both of these descending pathways contain neurons that are responsive to conspecific song.Solis, M.M., M.S. Brainard, N.A. Hessler and A.J. Doupe. 2000. Song selectivity and sensorimotor signals in vocal learning and production. Proceedings of the National Academy of Sciences USA 97:11836-11842. Female Canaries lost the ability to discriminate between conspecific and heterospecific song after bilateral lesions to the high vocal center HVC, a nucleus that sits at the apex of both pathways.Brenowitz, E.A. 1991. Altered perception of species-specific song by female birds after lesions of a forebrain nucleus. Science 251:303-304. In males, however, most song system neurons respond maximally to the sound of the bird's own song, even more than they do to the tutor's song or any other conspecific song.Margoliash, D., and M. Konishi. 1985. Auditory representation of autogenous song in the song system of white-crowned sparrows. Proceedings of the National Academy of Sciences USA 82:5997-6000.Margoliash, D. 1986. Preference for autogenous song by auditory neurons in a song system nucleus of the white-crowned sparrow. Journal of Neuroscience 13:4737-4747. In HVC, neurons switch from responding best to tutor song (35–69 days post-hatch) to responding best to the bird's own song (>70 days post-hatch).Nick, T.A., and M. Konishi. 2005. Neural song preference during vocal learning in the zebra finch depends on age and state. Journal of Neurobiology 62:231-242. Song preferences of neurons in these pathways are important for sensorimotor learning, however several lines of evidence suggest that the specific ability to discriminate conspecific from heterospecific song does not reside in the AFP or the SMP. Most importantly, gene expression studies have demonstrated that, as a broad unit, neurons in the AFP and SMP show increased activation when a bird is singing, but not when it is simply listening to song.Jarvis, E.D., and F. Nottebohm. 1997. Motor-driven gene expression. Proceedings of the National Academy of Sciences USA 94:4097-4102. With the exception of female Canaries, the neural substrate for conspecific song preference is thought to reside outside the conventional song system, in the auditory pathway.Mello, C.V., D.S. Vicario and D.F. Clayton. 1992. Song presentation induces gene-expression in the songbird forebrain. Proceedings of the National Academy of Sciences 89:6818-6822.Bolhuis, J.J., G.G.O. Zijlstra, A.M. Den Boer-Visser and E.A. Van der Zee. 2000. Localized neuronal activation in the zebra finch brain is related to the strength of song learning. Proceedings of the National Academy of Sciences USA 97:2282-2285.
Auditory pathway
Cochlea Avian hair cells have been extensively studied in the cochlea of the barn owl,Konishi, M., T.T. Takahashi, H. Wagner, W.E. Sullivan and C.E. Carr. 1988. Neurophysiological and anatomical substrates of sound localization in the owl. In "Auditory Function". G.M. Edelman, W.E. Gall and W.M. Cowan, Eds. Wiley: New York. and it is now known that both the morphological structure of hair cell papillae and the ion channels that characterize hair cell membranes confer spectral tuning properties. Ca2+ dependent K+ channels are produced as splice variants of the cSlo gene,Rosenblatt, K.P., Z-P. Sun, S Heller and A.J. Hudspeth. 1997. Distribution of Ca2+-activated K+ channel isoforms along the tonotopic gradient of the chicken's cochlea. Neuron 19:1061-1075. and different isoforms cause the hair cell to preferentially respond to different resonant frequencies.Koppl, C., G.A. Manley and M. Konishi. 2000. Auditory processing in birds. Current Opinion in Neurobiology 10:474-481.Fettiplace, R. and P.A. Fuchs. 1999. Mechanisms of hair cell tuning. Annual Review of Physiology 61:809-834. Species-specific differences in cSlo isoforms of hair cell membranes may therefore play a role in the discrimination of conspecific and heterospecific notes in songbirds.
Auditory thalamus Studies on zebra finch have shown that nuclei in the auditory thalamus, two steps up from the cochlea, do not passively relay input from peripheral sensory structures into higher forebrain structures. Thalamic nuclei show different patterns of gene expression in response to different stimuli, implicating them in the process of acoustic discrimination.Brauth, S.E., W. Liang and W.S. Hall. 2006. Contact-call driven and tone-driven zenk expression in the nucleus ovoidalis of the budgerigar (Melopsittacus undulates). NeuroReport 17:1407-1410. Neurons in the nucleus ovoidalis (Ov) have receptive fields that are tuned to respond to the specific combination of spectral and temporal features present in syllables of conspecific song. Stimulus-selective tuning is determined by the receptor proteins and ion channels characterizing synapses of these neurons. Neurons can selectively respond to time-based differences between songs (e.g. syllable length or syllable-interval length) if they are post-synaptic to either fast-release (ionotropic) or slow-release (metabotropic) glutamate receptors.Dutar, P., J. Petrozzino and H. Vu. 2000. Slow synaptic inhibition mediated by metabotropic glutamate receptor activation of GIRK channels. Journal of Neurophysiology 84:2284-2290.Amin, N., P. Gill and F. Theunissen. 2010. Role of the zebra finch auditory thalamus in generating complex representations for natural sounds. Journal of Neurophysiology 104:784.
Auditory forebrain Strong conspecific-selective responses have been most consistently demonstrated in neurons of the higher-level structures of the auditory system: The caudomedial neostriatum (NCM),Bailey, D., and J. Rosebush. 2002. The hippocampus and caudomedial neostriatum show selective responsiveness to conspecific song in the female zebra finch. Journal of Neurobiology 52:43-51.George, I., H. Cousillas, and J. Richard. 2008. A potential neural substrate for processing functional classes of complex acoustic signals. PLoS ONE 3:e2203. the auditory thalamo-recipient subfield (Field L: L1, L2a, L2b, L3),Grace, J., N. Amin, and N. Singh. 2003. Selectivity for conspecific song in the zebra finch auditory forebrain. Journal of Neurophysiology 89:472-487. and the caudal mesopallium (CM: CMM and CLM).Boumans, T., C. Vignal and A. Smolders. 2008. Functional magnetic resonance imaging in zebra finch discerns the neural substrate involved in segregation of conspecific song from background noise. Journal of Neurophysiology 99:931-938.Chew, S., and D. Vicario. 1996. A large-capacity memory system that recognizes the calls and songs of individual birds. Proceedings of the National Academy of Sciences 93:1950-1955.Hsu, A., S. Woolley, T. Fremouw, and F. Theunissen. 2004. Modulation power and phase spectrum of natural sounds enhance neural encoding performed by single auditory neurons. The Journal of Neuroscience 24:9201.Gill, P., S. Woolley, T. Fremouw, and F. Theunissen. 2008. What's that sound? Auditory area CLM encodes stimulus surprise, not intensity or intensity changes. Journal of Neurophysiology 99:2809. NCM and CM have been known to be discussed in conjunction with one another being as they are functionally similar. Recent studies have begun to show that while that is true, CM seems to respond in a manner relative to whether or not the stimulus is personally significant to the bird.
In European starlings, neurons in NCM habituate to a particular stimulus, and "remember" individual characteristics of songs to which a bird was exposed. This indicates that NCM functions in individual recognition, through the strategic recruitment of N-Methyl-D-aspartate receptors (NMDAR) to synapses that receive repeated patterns of excitation.George, I., H. Cousillas, and J. Richard. 2008. A potential neural substrate for processing functional classes of complex acoustic signals. PLoS ONE 3:e2203. In fact, NMDARs are thought to be the unit broadly responsible for synaptic memory in the central nervous system. NMDARs in NCM neurons, therefore, might be a compelling target for selection when song functions in discrimination among conspecific songs, for neighbor recognition and territorial defense, but NCM is unlikely to play a role in the discrimination of conspecific from heterospecific songs.