Bellwethers of change: population modelling of North Pacific humpback whales from 2002 through 2021 reveals shift from recovery to climate response.

For the 40 years after the end of commercial whaling in 1976, humpback whale populations in the North Pacific Ocean exhibited a prolonged period of recovery. Using mark-recapture methods on the largest individual photo-identification dataset ever assembled for a cetacean, we estimated annual ocean-basin-wide abundance for the species from 2002 through 2021. Trends in annual estimates describe strong post-whaling era population recovery from 16 875 (± 5955) in 2002 to a peak abundance estimate of 33 488 (± 4455) in 2012. An apparent 20% decline from 2012 to 2021, 33 488 (± 4455) to 26 662 (± 4192), suggests the population abruptly reached carrying capacity due to loss of prey resources. This was particularly evident for humpback whales wintering in Hawai'i, where, by 2021, estimated abundance had declined by 34% from a peak in 2013, down to abundance levels previously seen in 2006, and contrasted to an absence of decline in Mainland Mexico breeding humpbacks. The strongest marine heatwave recorded globally to date during the 2014-2016 period appeared to have altered the course of species recovery, with enduring effects. Extending this time series will allow humpback whales to serve as an indicator species for the ecosystem in the face of a changing climate.

Diel spatio-temporal patterns of humpback whale singing on a high-density breeding ground.

Humpback whale song chorusing dominates the marine soundscape in Hawai'i during winter months, yet little is known about spatio-temporal habitat use patterns of singers. We analysed passive acoustic monitoring data from five sites off Maui and found that ambient noise levels associated with song chorusing decreased during daytime hours nearshore but increased offshore. To resolve whether these changes reflect a diel offshore-onshore movement or a temporal difference in singing activity, data from 71 concurrently conducted land-based theodolite surveys were analysed. Non-calf pods (n = 3082), presumably including the majority of singers, were found further offshore with increasing time of the day. Separately, we acoustically localized 217 nearshore singers using vector-sensors. During the day, distances to shore and minimum distances among singers increased, and singers switched more between being stationary and singing while travelling. Together, these findings suggest that the observed diel trends in humpback whale chorusing off Maui represent a pattern of active onshore-offshore movement of singers. We hypothesize that this may result from singers attempting to reduce intraspecific acoustic masking when densities are high nearshore and avoidance of a loud, non-humpback, biological evening chorus offshore, creating a dynamic of movement of singers aimed at increasing the efficiency of their acoustic display.

A collaborative and near-comprehensive North Pacific humpback whale photo-ID dataset.

We present an ocean-basin-scale dataset that includes tail fluke photographic identification (photo-ID) and encounter data for most living individual humpback whales (Megaptera novaeangliae) in the North Pacific Ocean. The dataset was built through a broad collaboration combining 39 separate curated photo-ID catalogs, supplemented with community science data. Data from throughout the North Pacific were aggregated into 13 regions, including six breeding regions, six feeding regions, and one migratory corridor. All images were compared with minimal pre-processing using a recently developed image recognition algorithm based on machine learning through artificial intelligence; this system is capable of rapidly detecting matches between individuals with an estimated 97-99% accuracy. For the 2001-2021 study period, a total of 27,956 unique individuals were documented in 157,350 encounters. Each individual was encountered, on average, in 5.6 sampling periods (i.e., breeding and feeding seasons), with an annual average of 87% of whales encountered in more than one season. The combined dataset and image recognition tool represents a living and accessible resource for collaborative, basin-wide studies of a keystone marine mammal in a time of rapid ecological change.

Understanding across the senses: cross-modal studies of cognition in cetaceans.

Cross-modal approaches to the study of sensory perception, social recognition, cognition, and mental representation have proved fruitful in humans as well as in a variety of other species including toothed whales in revealing equivalencies that suggest that different sensory stimuli associated with objects or individuals may effectively evoke mental representations that are, respectively, object based or individual based. Building on established findings of structural equivalence in the form of spontaneous recognition of complex shapes across the modalities of echolocation and vision and behavior favoring identity echoic-visual cross-modal relationships over associative echoic-visual cross-modal relationships, examinations of transitive inference equivalencies from initially learned associations of visual and acoustic stimuli, and recent work examining spontaneous cross-modal social recognition of individual identity across acoustic and gustatory chemical modalities (i.e., the equivalence relationships among an individual's characteristics), we examine the history, utility and implications for cross-modal research in cetacean cognition. Drawing from research findings on bottlenose dolphins and beluga whales as well as other species we suggest future directions for cetacean cross-modal research to further illuminate understanding how structural and individual sensory equivalencies lead to object-centered and individual-centered mental representations, as well as to explore the potential for practical applications related to cetacean conservation.

Variations in received levels on a sound and movement tag on a singing humpback whale: Implications for caller identification.

Bio-logging devices are advancing the understanding of marine animal behavior, but linking sound production and behavior of individual baleen whales is still unreliable. Tag placement potentially within the near field of the sound source creates uncertainty about how tagged animal sounds will register on recorders. This study used data from a tagged singing humpback whale to evaluate this question of how sound levels present on a tag when calls are produced by a tagged animal. Root-mean-square (rms) received levels (RLs) of song units ranged from 112 to 164 dB re 1 µPa rms, with some, but not all, of the lower frequency units registering on the tag's 800 Hz accelerometer sensor. Fifty-nine percent of recorded units measured lower acoustic RLs than previously reported source levels for humpback song, but signal-to-noise ratios (SNRs) were 30-45 dB during periods of the dive with low noise. This research highlights that tag RL does not alone predict caller identity, argues for higher SNR thresholds if using SNR to inform decisions about the source of a call, and provides a baseline for future research identifying diagnostic properties of tagged animal calls in cetacean bioacoustic tag datasets.

Corticosterone in central North Pacific male humpback whales (Megaptera novaeangliae): Pairing sighting histories with endocrine markers to assess stress.

Developing a better understanding of the stress response is critical to ensuring the health and sustainability of marine mammal populations. However, accurately measuring and interpreting a stress response in free-ranging, large cetaceans is a nascent field. Here, an enzyme immunoassay for corticosterone was validated for use in biopsy samples from male humpback whales (Megaptera novaeangliae). Analyses were conducted on 247 male North Pacific humpback whale blubber samples, including 238 non-calves and 9 calves that were collected on the Hawaiian breeding and Southeast Alaskan feeding grounds from 2004 to 2006. Significant relationships were found when corticosterone concentrations were examined by year, age class and distribution between locations. When examined by year, corticosterone concentrations for male humpback whales were higher in Hawaii in 2004 than in 2005 and 2006 (p < 0.05). Corticosterone concentration also varied by age class with initially high concentrations at birth which subsequently tapered off and remained relatively low until sexual maturity was reached around age 8-10 years. Corticosterone concentrations appeared to peak in male humpback whales around 15-25 years of age. Blubber biopsies from Alaska and Hawaii had similar mean corticosterone concentrations, yet the variability in these samples was much greater for whales located in Hawaii. It is clear that much work remains to be done in order to accurately define or monitor a stress response in male humpback whales and that specific attention is required when looking at age, sex, and yearly trends. Our results suggest that a stress response may be most impacted by age and yearly oceanographic conditions and needs to be initially examined at the individual level.

Testosterone trends within and across seasons in male humpback whales (Megaptera novaeangliae) from Hawaii and Alaska.

Understanding reproductive profiles and timing of reproductive events is essential in the management and conservation of humpback whales (Megaptera novaeangliae). Yet compared to other parameters and life history traits, such as abundance, migratory trends, reproductive rates, behavior and communication, relatively little is known about variations in reproductive physiology, especially in males. Here, an enzyme immunoassay (EIA) for testosterone was validated for use in biopsy samples from male humpback whales. Analyses were conducted on 277 North Pacific male humpback whale blubber samples, including 268 non-calves and 9 calves that were collected in the Hawaiian breeding grounds and the Southeast Alaskan feeding grounds from 2004 to 2006. Testosterone concentrations (ng/g) were significantly different between non-calves sampled in Hawaii (n = 182) and Alaska (n = 86, p < 0.05) with peak testosterone concentrations occurring in the winter (January-March) and the lowest concentrations occurring in the summer (June-September). Fall and spring showed increasing and decreasing trends in testosterone concentrations, respectively. Blubber testosterone concentrations in non-calves and calves sampled in Alaska were not significantly different. Blubber and skin from the same individual biopsies (n = 37) were also compared, with blubber having significantly higher testosterone concentrations (p < 0.05) than skin samples. We found variability in testosterone concentration with age, suggesting that male humpbacks reach peak lifetime testosterone concentrations in the breeding grounds around age 8-25 years. The testosterone profile of male humpback whales follows a predictable pattern for capital breeders, where testosterone begins to increase prior to the breeding season, stimulating the onset of spermatogenesis. Incorporation of reproductive hormonal profiles into our overall understanding of humpback whale physiology will shed additional light on the timing of reproduction and overall health of the recently delisted Hawaii distinct population segment (DPS).

The effect of isolation, fragmentation, and population bottlenecks on song structure of a Hawaiian honeycreeper.

Little is known about how important social behaviors such as song vary within and among populations for any of the endemic Hawaiian honeycreepers. Habitat loss and non-native diseases (e.g., avian malaria) have resulted in isolation and fragmentation of Hawaiian honeycreepers within primarily high elevation forests. In this study, we examined how isolation of Hawai'i 'amakihi (Chlorodrepanis virens) populations within a fragmented landscape influences acoustic variability in song. In the last decade, small, isolated populations of disease tolerant 'amakihi have been found within low elevation forests, allowing us to record 'amakihi songs across a large elevational gradient (10-1800 m) that parallels disease susceptibility on Hawai'i island. To understand underlying differences among populations, we examined the role of geographic distance, elevation, and habitat structure on acoustic characteristics of 'amakihi songs. We found that the acoustic characteristics of 'amakihi songs and song-type repertoires varied most strongly across an elevational gradient. Differences in 'amakihi song types were primarily driven by less complex songs (e.g., fewer frequency changes, shorter songs) of individuals recorded at low elevation sites compared to mid and high elevation populations. The reduced complexity of 'amakihi songs at low elevation sites is most likely shaped by the effects of habitat fragmentation and a disease-driven population bottleneck associated with avian malaria, and maintained through isolation, localized song learning and sharing, and cultural drift. These results highlight how a non-native disease through its influence on population demographics may have also indirectly played a role in shaping the acoustic characteristics of a species.

Exodus! Large-scale displacement and social adjustments of resident Atlantic spotted dolphins (Stenella frontalis) in the Bahamas.

Over the last 20 years, significant habitat shifts have been documented in some populations of cetaceans. On Little Bahama Bank (LBB) there are sympatric communities of resident Atlantic spotted dolphins (Stenella frontalis) and bottlenose dolphins (Tursiops truncatus), monitored since 1985. The size and social structure (three clusters: Northern, Central, Southern) have been stable among the spotted dolphin community with little immigration/emigration, even after large demographic losses (36%) following two major hurricanes in 2004. In 2013 an unprecedented exodus of over 50% (52 individuals) of the spotted dolphin community was documented. The entire Central cluster and a few Northern and Southern individuals relocated 161 km south to Great Bahama Bank (GBB), also home to two sympatric resident communities of spotted dolphins and bottlenose dolphins. During the late summer of 2013 and the summers of 2014 and 2015 both sites were regularly monitored but no former LBB dolphins returned to LBB. Uncharacteristic matriline splits were observed. Social analyses revealed random associations for those spotted dolphins and very little integration between spotted dolphins that moved to GBB (MGBB) and those dolphin resident to GBB (RGBB). Male alliances among spotted dolphins were present, with some altered patterns. On LBB, the operational sex ratio (OSR) was reduced (.40 to .25). OSR for MGBB and RGBB dolphins were similar (.45 and .43). A significant steady decrease in sea surface temperature and chlorophyll a (a proxy for plankton production) occurred on LBB leading up to this exodus. Similar trends were not present over the same period on GBB. The sudden large-scale shift of spotted dolphins from LBB to GBB in association with the gradual decline in certain environmental factors suggests that a possible "tipping point" was reached in prey availability. This study provides a unique view into social and genetic implications of large-scale displacement of stable dolphin communities.

Measurements of humpback whale song sound levels received by a calf in association with a singer.

Male humpback whales produce loud "songs" on the wintering grounds and some sing while escorting mother-calf pairs, exposing them to near-continuous sounds at close proximity. An Acousonde acoustic and movement recording tag deployed on a calf off Maui, Hawaii captured sounds produced by a singing male escort. Root-mean-square received levels ranged from 126 to 158 dB re 1 µPa. These levels represent rare direct measurements of sound to which a newly born humpback calf may be naturally exposed by a conspecific, and may provide a basis for informed decisions regarding anthropogenic sound levels projected near calves.

Humpback whale populations share a core skin bacterial community: towards a health index for marine mammals?

Microbes are now well regarded for their important role in mammalian health. The microbiology of skin--a unique interface between the host and environment--is a major research focus in human health and skin disorders, but is less explored in other mammals. Here, we report on a cross-population study of the skin-associated bacterial community of humpback whales (Megaptera novaeangliae), and examine the potential for a core bacterial community and its variability with host (endogenous) or geographic/environmental (exogenous) specific factors. Skin biopsies or freshly sloughed skin from 56 individuals were sampled from populations in the North Atlantic, North Pacific and South Pacific oceans and bacteria were characterized using 454 pyrosequencing of SSU rRNA genes. Phylogenetic and statistical analyses revealed the ubiquity and abundance of bacteria belonging to the Flavobacteria genus Tenacibaculum and the Gammaproteobacteria genus Psychrobacter across the whale populations. Scanning electron microscopy of skin indicated that microbial cells colonize the skin surface. Despite the ubiquity of Tenacibaculum and Psychrobater spp., the relative composition of the skin-bacterial community differed significantly by geographic area as well as metabolic state of the animals (feeding versus starving during migration and breeding), suggesting that both exogenous and endogenous factors may play a role in influencing the skin-bacteria. Further, characteristics of the skin bacterial community from these free-swimming individuals were assembled and compared to two entangled and three dead individuals, revealing a decrease in the central or core bacterial community members (Tenacibaculum and Psychrobater spp.), as well as the emergence of potential pathogens in the latter cases. This is the first discovery of a cross-population, shared skin bacterial community. This research suggests that the skin bacteria may be connected to humpback health and immunity and could possibly serve as a useful index for health and skin disorder monitoring of threatened and endangered marine mammals.

Predictive modeling of spinner dolphin (Stenella longirostris) resting habitat in the main Hawaiian Islands.

Predictive habitat models can provide critical information that is necessary in many conservation applications. Using Maximum Entropy modeling, we characterized habitat relationships and generated spatial predictions of spinner dolphin (Stenella longirostris) resting habitat in the main Hawaiian Islands. Spinner dolphins in Hawai'i exhibit predictable daily movements, using inshore bays as resting habitat during daylight hours and foraging in offshore waters at night. There are growing concerns regarding the effects of human activities on spinner dolphins resting in coastal areas. However, the environmental factors that define suitable resting habitat remain unclear and must be assessed and quantified in order to properly address interactions between humans and spinner dolphins. We used a series of dolphin sightings from recent surveys in the main Hawaiian Islands and a suite of environmental variables hypothesized as being important to resting habitat to model spinner dolphin resting habitat. The model performed well in predicting resting habitat and indicated that proximity to deep water foraging areas, depth, the proportion of bays with shallow depths, and rugosity were important predictors of spinner dolphin habitat. Predicted locations of suitable spinner dolphin resting habitat provided in this study indicate areas where future survey efforts should be focused and highlight potential areas of conflict with human activities. This study provides an example of a presence-only habitat model used to inform the management of a species for which patterns of habitat availability are poorly understood.

Recurring patterns in the songs of humpback whales (Megaptera novaeangliae).

Humpback whales, unlike most mammalian species, learn new songs as adults. Populations of singers progressively and collectively change the sounds and patterns within their songs throughout their lives and across generations. In this study, humpback whale songs recorded in Hawaii from 1985 to 1995 were analyzed using self-organizing maps (SOMs) to classify the sounds within songs, and to identify sound patterns that were present across multiple years. These analyses supported the hypothesis that recurring, persistent patterns exist within whale songs, and that these patterns are defined at least in part by acoustic relationships between adjacent sounds within songs. Sound classification based on acoustic differences between adjacent sounds yielded patterns within songs that were more consistent from year to year than classifications based on the properties of single sounds. Maintenance of fixed ratios of acoustic modulation across sounds, despite large variations in individual sounds, suggests intrinsic constraints on how sounds change within songs. Such acoustically invariant cues may enable whales to recognize and assess variations in songs despite propagation-related distortion of individual sounds and yearly changes in songs.

Sound production by singing humpback whales.

Sounds from humpback whale songs were analyzed to evaluate possible mechanisms of sound production. Song sounds fell along a continuum with trains of discrete pulses at one end and continuous tonal signals at the other. This graded vocal repertoire is comparable to that seen in false killer whales [Murray et al. (1998). J. Acoust. Soc. Am. 104, 1679-1688] and human singers, indicating that all three species generate sounds by varying the tension of pneumatically driven, vibrating membranes. Patterns in the spectral content of sounds and in nonlinear sound features show that resonating air chambers may also contribute to humpback whale sound production. Collectively, these findings suggest that categorizing individual units within songs into discrete types may obscure how singers modulate song features and illustrate how production-based characterizations of vocalizations can provide new insights into how humpback whales sing.

Neuroglial modulation in peripheral sensory systems.

Glia are increasingly appreciated as active participants in central neural processing via calcium waves, electrical coupling, and even synaptic-like release of "neuro"-transmitters. In some sensory organs (e.g., retina, olfactory bulb), glia have been shown to interact with neurons in the same manner, although their role in perception has yet to be elucidated. In the organ of Corti, synapses occur between supporting cells and neurons. In one sensory organ, the Pacinian corpuscle (fine touch), glia have been shown to play just as important a role in sensory transduction as they do in neural processing in the brain, and the functional role is quite clear; the modified Schwann cells of the capsule are responsible for the rapid adaptation process of the PCs, integral to its function as a vibration detector. This complex glial/neuronal relationship may be a recent evolutionary phenomenon and may account for much of the relative sophistication of vertebrate nervous systems.

GABAergic/glutamatergic-glial/neuronal interaction contributes to rapid adaptation in pacinian corpuscles.

Pacinian corpuscles (PCs) are tactile receptors composed of a nerve ending (neurite) that is encapsulated by layers of lamellar cells. PCs are classified as primary mechanoreceptors because there is no synapse between the transductive membrane and the site of action-potential generation. These touch receptors respond in a rapidly adapting manner to sustained pressure (indentation or displacement), which until now was believed to be attributable solely to the mechanical properties of the capsule. However, evidence of positive immunoreactivity for GABA receptors on the neurite, as well as evidence for gene expression of synaptobrevin in the lamellar cells led to the hypothesis that GABAergic inhibition originating from the lamellar cells is involved in the rapid adaptation process of PCs. Electrophysiological data from isolated PCs demonstrates that, in the presence of either gabazine or picrotoxin (GABA receptor antagonists), many action potentials appear during the static portion of a sustained indentation stimulus (similar to slowly adapting receptors) and that these "static" spikes completely disappear in the presence of GABA. It was consequently hypothesized that glutamate, released by either the neurite itself or the lamellar cells, caused these action potentials. Indeed, the glutamate receptor blocker kynurenate either decreased or totally eliminated the static spikes. Together, these results suggest that GABA, emanating from the modified Schwann cells of the capsule, inhibits glutamatergic excitation during the static portion of sustained pressure, thus forming a "mechanochemical," rather than purely mechanical, rapid adaptation response. This glial-neuronal interaction is a completely novel finding for the PC.

The effects of sound conditioning on gentamicin-induced vestibulocochlear toxicity in gerbils.

OBJECTIVES/HYPOTHESIS: Recent studies in animal models have shown via physiologic and histologic measures that the administration of exogenous antioxidants is protective against gentamicin-induced oto-vestibulo toxicity. In addition, studies have also shown that sound conditioning increases cochlear antioxidants. The objective of this study is to determine whether sound conditioning provides protection against gentamicin in the cochlear and/or vestibular system. STUDY DESIGN: : Prospective animal study. METHODS: Three-month-old gerbils were divided into three groups (A, B, and C). The gerbils in group A were sound conditioned only (n = 2). In group B, the animals received gentamicin on the round window (n = 2). The gerbils in group C were sound conditioned first and later received gentamicin to the round window (n = 2). The animals were ultimately sacrificed and their right cochlea and posterior crista ampullaris were removed, processed, and sectioned. The specimens were analyzed for inner hair cell (IHC) and outer hair cell (OHC) loss and vestibular supporting and sensory hair cell nuclei per micrometer of vestibular epithelium. RESULTS: The sound-conditioned group (A) had no loss of cochlear hair cells. The gerbils treated with gentamicin only (B) had a 34% decrease of OHCs and 49% decrease of IHCs. The sound-conditioned plus gentamicin-treated group (C) had a 5.5% decrease in OHCs and 12% decrease in IHCs. There were no significant differences with regards to supporting cell nuclei within the posterior crista across all groups. When compared to group A, the gerbils in groups B and C did have a 23 to 42% decrease in the number of sensory cell nuclei per micrometer of vestibular epithelium. CONCLUSIONS: Sound conditioning does appear to attenuate the effects of gentamicin in the cochlea, although not significantly altering its vestibulotoxicity. An upregulation of cochlear-specific antioxidants is believed to be an important factor. As we had a small sample size, we can only note trends in the data, but future studies with more animals and measurements of antioxidant levels after sound conditioning would be useful to quantify this effect and determine if it can be exploited clinically. Laryngoscope, 2009.

A claim in search of evidence: reply to Manger's thermogenesis hypothesis of cetacean brain structure.

In a recent publication in Biological Reviews, Manger (2006) made the controversial claim that the large brains of cetaceans evolved to generate heat during oceanic cooling in the Oligocene epoch and not, as is the currently accepted view, as a basis for an increase in cognitive or information-processing capabilities in response to ecological or social pressures. Manger further argued that dolphins and other cetaceans are considerably less intelligent than generally thought. In this review we challenge Manger's arguments and provide abundant evidence that modern cetacean brains are large in order to support complex cognitive abilities driven by social and ecological forces.

Mesenteric and tactile Pacinian corpuscles are anatomically and physiologically comparable.

Pacinian corpuscles (PCs) in cat mesentery have been studied extensively to help determine the structural and functional bases of tactile mechanotransduction. Although we, like many other investigators, have found that the mesenteric receptors are anatomically very similar to those found in mammalian skin, few physiological characteristics of the mesenteric PCs and those of the skin have been compared. Action-potential rate-amplitude and frequency characteristics (10 Hz-1 KHz), as well as interval (IH) and peri-stimulus-time (PSTH) histograms in response to sinusoidal displacements were obtained from nerve fibers innervating mesenteric PCs and from PC fibers innervating cat glabrous skin. The intensity characteristics obtained on both preparations showed similar response profiles, including equal slopes for low stimulus intensities (approximately 10, with impulse ratios/20 dB displacement) and one and two impulse/cycle entrainment. The frequency characteristics of both groups were U-shaped with similar low-frequency slopes (-12.5 dB/octave) and bandwidths (Q(3dB) = 1.4). The best frequency for both the tactile PCs' and mesenteric PCs was 250 Hz, which is in the expected range. The IHs showed entrainment and the PSTHs showed neither transient responses nor adaptation to steady-state sinusoidal stimuli. The functional similarity between mesenteric PCs' nerve responses and those of tactile PC afferents, as well as the receptors' anatomical similarity, lead us to suggest that the mesenteric PC can act as a model for those in the skin. Furthermore, since the frequency characteristics of the two PC types are similar, it is concluded that the skin, while attenuating stimulus intensity, does not impart temporal filtering of vibratory stimuli.

Localization of Merkel cells in the monkey skin: an anatomical model.

The Merkel cell-neurite complex is considered to be one class of mechanoreceptors in the skin. Merkel cells are innervated by slowly adapting type I (SAI) tactile nerve fibers. In this paper, the detailed distribution of Merkel cells is studied by immunohistochemical labeling of the monkey (Macaca fascicularis) digital glabrous skin. Specific morphometric variables (density of intermediate epidermal ridges and Merkel cells, distance between skin surface and ridge tips and bases, maximum and average cell counts per ridge, distance between cells and ridges) were measured by a combination of light/fluorescence microscopy and computer-image analysis. The morphometric results were similar for each digit of the monkey's hand. Next, the anatomical data were used to form a three-dimensional reconstruction of the Merkel-cell distribution in the fingertip skin. A patch of the distal-pad surface was then computationally flattened to obtain the two-dimensional distribution of Merkel cells. Based on previous anatomical and physiological data, SAI fibers were simulated to innervate clusters of Merkel cells in the distal-pad surface. On average, 28 cells were innervated by a single fiber. The resulting anatomical model may be used to estimate the population response of SAI fibers by incorporating spike generation.