Sound sensitivity of neurons in rat hippocampus during performance of a sound-guided task

Sound sensitivity of neurons in rat hippocampus during performance of a sound-guided task Itskov Vinnik Honey Schnupp Diamond

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Sound sensitivity of neurons in rat hippocampus during performance of a sound-guided task 2012 Journal of Neurophysiology 10.1152/jn.00404.2011 Itskov2012-sound-sensitivity-of-neurons-in-rat-hippocam Itskov2012-sound-sensitivity-of-neurons-in-rat-hippocam.txt, the project's staged copy 0dfaed68f29ef86afa1349ce9aef8af05d516a22 not-redistributable neuroscience

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0 spans located by searching the stored text for the quote's exact words, allowing any whitespace between them whether hippocampal neurons encode a sound itself, once every difference in what the animal does about it has been designed away Quotation withheld because this record is not cleared for redistribution. whether a stimulus representation in hippocampus can be separated from the position and movement responses that always accompany stimulus-guided behaviour Quotation withheld because this record is not cleared for redistribution. sound identity is encoded by 21 percent of neurons, independently of response direction, only on one platform at a time, and not at all when the same sounds are heard outside the task Quotation withheld because this record is not cleared for redistribution. existence Quotation withheld because this record is not cleared for redistribution. sound coding in hippocampal CA1 neurons Quotation withheld because this record is not cleared for redistribution. electrophysiology electrophysiology Quotation withheld because this record is not cleared for redistribution. mechanisms the hippocampus binds salient sensory events to the spatial context in which they occur, producing location-specific 'object in place' representations rather than context-free sound representations Quotation withheld because this record is not cleared for redistribution. mechanisms the animals build two separate task representations, one per platform, which is why the learned contingencies did not transfer immediately between locations Quotation withheld because this record is not cleared for redistribution. sound coding is contingent on the animal's location, since a neuron that separates a sound pair on one platform often fails to separate the same pair on the other Quotation withheld because this record is not cleared for redistribution. and contingent on the sounds meaning something, since nothing survives when the same sounds are played outside the task Quotation withheld because this record is not cleared for redistribution. sound identity and response direction are carried by populations that overlap only as much as chance predicts Quotation withheld because this record is not cleared for redistribution. the pattern fits an object-in-place account in which the hippocampus binds salient events to the context they occurred in Quotation withheld because this record is not cleared for redistribution. the failure to transfer the task to the second platform suggests two separate task representations, or a conflict between room-centred and self-centred frames Quotation withheld because this record is not cleared for redistribution. Too few error trials were available to test whether sound representations were the same on correct and incorrect trials. what this limits: any claim that the sound representation is what drives the correct choice: THERE WERE INSUFFICIENT NUMBERS OF ERROR TRIALS TO PERMIT AN ANALYSIS OF WHETHER THE REPRESENTATION OF SPECIFIC SOUNDS WAS EQUIVALENT ON CORRECT AND INCORRECT TRIALS Quotation withheld because this record is not cleared for redistribution. The pyramidal-cell versus interneuron split rests on extracellular physiological criteria, which cannot definitively identify cell type. what this limits: every result reported by cell type: WE STRESS THAT A DEFINITIVE CLASSIFICATION OF CELL TYPES REQUIRES INFORMATION BEYOND THAT WHICH CAN BE OBTAINED WITH EXTRACELLULAR RECORDINGS ALONE Quotation withheld because this record is not cleared for redistribution. The study was not designed to map which sounds a neuron prefers across space, only whether sound sensitivity transfers between locations. what this limits: the sound-by-place interaction: OUR EXPERIMENT WAS NOT DESIGNED TO MAP SOUND PREFERENCES ACROSS SPACE, though the results are read as confirming and extending earlier findings Quotation withheld because this record is not cleared for redistribution. there were too few error trials to ask whether the sound representation is the same when the animal gets it wrong what this limits: the same scope as limitations[0] - the correct/incorrect comparison could not be run Quotation withheld because this record is not cleared for redistribution. a definitive classification of cell types needs more than extracellular recording can give what this limits: the same scope as limitations[1] - the pyramidal/interneuron split is physiological, not definitive Quotation withheld because this record is not cleared for redistribution. the differences between the two physiologically distinguished cell types were statistically highly significant but nevertheless not very large what this limits: the cell-type difference, whose statistics and whose meaning are separated explicitly: THESE DIFFERENCES WERE STATISTICALLY HIGHLY SIGNIFICANT, BUT THEIR NEUROANATOMICAL AND FUNCTIONAL SIGNIFICANCE REMAINS DIFFICULT to assess Quotation withheld because this record is not cleared for redistribution. the experiment was not designed to map sound preferences across space what this limits: the same scope as limitations[2], against the odour literature where responses OFTEN DIFFERED AT DIFFERENT LOCATIONS Quotation withheld because this record is not cleared for redistribution. sessions were discarded wherever reaction times differed between the two sounds sharing a response, removing 168 of 429 neurons from analysis what this limits: the sound-difference result: Quotation withheld, so behaviour is controlled by discarding sessions Quotation withheld because this record is not cleared for redistribution. Shannon's mutual information is adopted as the measure of stimulus-response dependence in spike trains, chosen over conventional statistical tests because it yields a common scale across experiments Quotation withheld because this record is not cleared for redistribution. mutual information with a bias correction, chosen for a uniform scale comparable across experiments Quotation withheld because this record is not cleared for redistribution. artificial vowels, chosen as a more naturalistic class of stimuli than pure tones Quotation withheld because this record is not cleared for redistribution. a published discrimination threshold, used to set the formant spacing well above where rats reach plateau performance Quotation withheld because this record is not cleared for redistribution. the L-ratio and isolation index as cluster separation measures, applied on top of manual inspection Quotation withheld because this record is not cleared for redistribution. the two sounds paired with EACH response direction compared against one another, so the comparison is within a single behavioural response eliminates: the animal's behaviour as the explanation of a firing difference - two sounds that lead to different actions differ in what the rat DOES as well as in what it HEARS, and a hippocampal difference would then be about movement · outcome (stated by the tagger, no quotation): held Quotation withheld because this record is not cleared for redistribution. THE CONFOUND IS DESIGNED AWAY RATHER THAN CORRECTED FOR: two sounds share each action, so any firing difference between them cannot be the behaviour - it must be the stimulus Quotation withheld because this record is not cleared for redistribution. and the same task is run on two identical platforms in different places, which turns spatial context from a nuisance into a manipulated variable Quotation withheld because this record is not cleared for redistribution. DATA ARE DISCARDED TO PROTECT THE INFERENCE: every session where the two sounds produced different reaction times was thrown out, so no motor difference can be read as a stimulus response Quotation withheld because this record is not cleared for redistribution. and the criterion for direction sensitivity requires all four stimulus pairings to be significant, precisely so that a sound-driven response cannot masquerade as a direction response Quotation withheld because this record is not cleared for redistribution. A TEST OF THE TEST: the distribution of per-neuron p values across the whole population is compared against a shuffled distribution, to ask whether the count of significant neurons exceeds what false positives would give Quotation withheld because this record is not cleared for redistribution. THE MEASURE IS CHOSEN BECAUSE IT MAKES RESULTS JOINABLE: information theory is picked over ANOVA or discriminant analysis because it provides a uniform scale that can be used to compare results from different experiments Quotation withheld because this record is not cleared for redistribution. THE NULL IS BACKED FOUR WAYS: the count is at the false-alarm rate, the population meta-test is null, the effect size is smaller, and visual inspection finds nothing convincing Quotation withheld because this record is not cleared for redistribution. A DISAGREEMENT BETWEEN LITERATURES IS ATTRIBUTED TO A VARIABLE ONE OF THEM NEVER VARIED: human hippocampal neurons look context-invariant, and in those studies the subjects were always tested in just a single location Quotation withheld because this record is not cleared for redistribution. and the contribution is measuring something a predecessor asserted - the independence of the overlapping assemblies was proposed but never demonstrated quantitatively Quotation withheld because this record is not cleared for redistribution. claim_type: existence a second reading reaching the same value. Recorded: existence — note: a second reading reaching the same value from a different sentence. Not applied - a person decides. Quotation withheld because this record is not cleared for redistribution. method: four sounds mapped onto two actions so that two stimuli always share a response, the same task repeated on two identical platforms, and mutual information between firing and either sound identity or turn direction a second reading DIFFERING from the recorded value. Recorded: electrophysiology — note: a second reading, verbatim-verified, disagreeing with the value on the record. Not applied - a person decides. Quotation withheld because this record is not cleared for redistribution. phenomenon: non-spatial sensory coding in a structure whose dominant signal is position a second reading DIFFERING from the recorded value. Recorded: sound coding in hippocampal CA1 neurons — note: a second reading, verbatim-verified, disagreeing with the value on the record. Not applied - a person decides. Quotation withheld because this record is not cleared for redistribution. extends → Itskov et al. (2011), the same group's tactile-stimulus hippocampus study Quotation withheld because this record is not cleared for redistribution. extends → Sakurai (1994, 1996, 2002) Quotation withheld because this record is not cleared for redistribution. extends → the authors' own tactile result, in which hippocampal responses to surfaces were location-dependent and independent of the action Quotation withheld because this record is not cleared for redistribution. qualifies → operant conditioning studies of hippocampal sound responses, where stimulus and conditioned response are coupled and cannot be told apart Quotation withheld because this record is not cleared for redistribution. extends → Sakurai's proposal of independent coding across overlapping assemblies, which was never demonstrated quantitatively Quotation withheld because this record is not cleared for redistribution. supports → odour studies reporting that hippocampal responses differ between locations Quotation withheld because this record is not cleared for redistribution. contradicts → the context-independent, categorical picture from human hippocampal single units Quotation withheld because this record is not cleared for redistribution. supports → the object-in-place account of hippocampal function Quotation withheld because this record is not cleared for redistribution. stimulus —distinct-from→ direction stimulus direction differs in: THE AXIS IS A DESIGN THAT MAKES THE ALTERNATIVE IMPOSSIBLE. 'Quotation withheld' Stimulus and behaviour are not separated by a measurement but by a PAIRING CHOSEN SO THEY CANNOT COVARY - the strongest form of dissociation, and one that a reader cannot check without knowing the pairing. · strength of the relation: 1 · note: THE CONFOUND IS DESIGNED AWAY: two stimuli share each response, so a firing difference between them must reflect the coding of stimulus identity rather than any aspect of behavior Audit 2026-09-28: DOUBTFUL - read against its span and kept, but the span dissociates stimulus from response direction; distinct-from is loose. Quotation withheld because this record is not cleared for redistribution. stimulus —distinct-from→ location stimulus location strength of the relation: 1 · note: and the same stimulus-reward pairing is carried out at different locations in the room, which turns spatial position from a nuisance into a manipulated variable Quotation withheld because this record is not cleared for redistribution. sound —distinct-from→ behavior sound behavior differs in: THE AXIS IS WHETHER THE SOUND IS TIED TO AN ACTION. 'Quotation withheld' A study playing sounds outside a task would find no auditory responses and conclude the hippocampus is not auditory - which is exactly the earlier result this paper's other rows are reconciling with. · strength of the relation: 1 · note: no coding for sound identity at all when the rats hear the same sounds outside the behavioural task Audit 2026-09-28: DOUBTFUL - read against its span and kept, but the span measures sound sensitivity independent of behaviour; distinct-from is loose. Quotation withheld because this record is not cleared for redistribution. platform —operationalised-as→ context platform context strength of the relation: 1 · note: two identical testing platforms at different locations in the same room, built to test the effect of spatial context on sound coding Audit 2026-09-28: DOUBTFUL - read against its span and kept, but platforms define contexts; operationalised-as is loose. Quotation withheld because this record is not cleared for redistribution. interneuron —contrasted-with→ pyramidal interneuron pyramidal differs in: THE AXIS IS THE PROPORTION THAT IS SOUND SENSITIVE, AND BOTH PROPORTIONS ARE NON-ZERO. 'Quotation withheld' A difference in RATE, not in kind - and the raw counts are given, so a reader can check what the percentages are of. · strength of the relation: 1 · note: 33 percent of putative interneurons sound sensitive against 16 percent of putative pyramidal cells, and more bits when they are Quotation withheld because this record is not cleared for redistribution. vowel —is-a→ sound vowel sound strength of the relation: 1 · note: chosen as a more naturalistic class of stimuli than pure tones, and already used all the way up the ascending pathway Quotation withheld because this record is not cleared for redistribution. mutual information mutual information Quotation withheld because this record is not cleared for redistribution. permutation test permutation test Quotation withheld because this record is not cleared for redistribution. Wilcoxon rank-sum test Wilcoxon rank-sum test Quotation withheld because this record is not cleared for redistribution. k-means clustering k-means clustering Quotation withheld because this record is not cleared for redistribution. confidence interval confidence interval Quotation withheld because this record is not cleared for redistribution. median and interquartile range median and interquartile range Quotation withheld because this record is not cleared for redistribution. sliding-window analysis sliding-window analysis Quotation withheld because this record is not cleared for redistribution. Wilcoxon rank sum test Wilcoxon rank sum test Quotation withheld because this record is not cleared for redistribution. mutual information mutual information Quotation withheld because this record is not cleared for redistribution. permutation test permutation test Quotation withheld because this record is not cleared for redistribution. binomial binomial Quotation withheld because this record is not cleared for redistribution. 55 of 261 tested CA1 neurons (21%) showed significant sensitivity to sound identity. Quotation withheld because this record is not cleared for redistribution. Sound-identity information was carried for only one response direction by 48 neurons, for two by 7, and for more than two by none. Quotation withheld because this record is not cleared for redistribution. When the same sounds were played outside the task, the proportion of sound-sensitive neurons fell to chance level, indicating no passive sound coding. Quotation withheld because this record is not cleared for redistribution. Sensitivity to sound identity and sensitivity to response direction were statistically independent properties of the same neuronal population. Quotation withheld because this record is not cleared for redistribution. Putative interneurons carried more sound-identity information while putative pyramidal cells carried more response-direction information. Quotation withheld because this record is not cleared for redistribution. The headline conclusion is that hippocampal sound coding is contingent on the sound being behaviourally meaningful rather than on its physical properties. Quotation withheld because this record is not cleared for redistribution. THE CONFOUND IS DESIGNED AWAY: two sounds share each action, so any firing difference between them must reflect stimulus identity rather than behaviour Quotation withheld because this record is not cleared for redistribution. and the same task is run on two identical platforms in different places Quotation withheld because this record is not cleared for redistribution. a stimulus representation can only be specified after teasing it apart from the position-dependent responses that accompany stimulus-guided behaviour Quotation withheld because this record is not cleared for redistribution. which is what makes earlier operant-conditioning work hard to interpret - stimulus and conditioned response are coupled Quotation withheld because this record is not cleared for redistribution. DATA ARE DISCARDED TO PROTECT THE INFERENCE: sessions where the two sounds gave different reaction times are excluded, at 14 percent of cases Quotation withheld because this record is not cleared for redistribution. leaving 261 of 429 recorded neurons in the analysis Quotation withheld because this record is not cleared for redistribution. 55 of 261 neurons (21 percent) carried significant sound identity information, at a median of 0.12 bits against a ceiling of 1.0 Quotation withheld because this record is not cleared for redistribution. A TEST OF THE TEST: the whole distribution of per-neuron p values was compared against a shuffled one, to ask whether the count of significant neurons exceeds the false-positive rate Quotation withheld because this record is not cleared for redistribution. AND THE DIRECTION CRITERION IS BUILT AGAINST A SPECIFIC ALTERNATIVE: all four stimulus pairings had to be significant, so a sound response cannot masquerade as a direction response Quotation withheld because this record is not cleared for redistribution. 113 of 261 neurons (43 percent) were sensitive to response direction, at a median of 0.22 bits Quotation withheld because this record is not cleared for redistribution. sound information appeared on only one of the two platforms in the large majority of cases Quotation withheld because this record is not cleared for redistribution. and the observed distribution across the four conditions matched an independence model derived by binomial expansion Quotation withheld because this record is not cleared for redistribution. whether a neuron was recruited for sound did not predict whether it was recruited for the action Quotation withheld because this record is not cleared for redistribution. THE PASSIVE CONDITION IS THE TEST OF WHETHER THE SOUND MATTERS AS A PHYSICAL SIGNAL OR AS A MEANINGFUL EVENT Quotation withheld because this record is not cleared for redistribution. AND THE NULL IS BACKED FOUR WAYS: 6 percent of neurons against a 5 percent false-alarm rate, a null population meta-test, a smaller effect size, and nothing convincing on visual inspection Quotation withheld because this record is not cleared for redistribution. so CA1 neurons were not sensitive to the same acoustic differences presented in isolation, even when they discriminated them inside the task Quotation withheld because this record is not cleared for redistribution. THE MEASURE IS CHOSEN BECAUSE IT MAKES RESULTS JOINABLE: information theory over ANOVA or discriminant analysis, for a uniform scale comparable across experiments Quotation withheld because this record is not cleared for redistribution. with an analytic bias correction whose validity condition on trial counts is checked Quotation withheld because this record is not cleared for redistribution. and a 200 ms window sliding in 25 ms steps, with multiple comparisons handled by a permutation test on the mean across time points Quotation withheld because this record is not cleared for redistribution. sound information first appeared at a median latency of 310 ms, and there were too few error trials to ask whether the representation survives a mistake Quotation withheld because this record is not cleared for redistribution. although the behavioral task and sound stimuli were identical, the transfer of the task to the second platform was not immediate, and the animals persistently achieved lower performance there Quotation withheld because this record is not cleared for redistribution. 33 percent of putative interneurons were sound sensitive against 16 percent of putative pyramidal cells, and carried more bits when they were Quotation withheld because this record is not cleared for redistribution. AND THE CLASSIFICATION IS DISOWNED IN THE SAME BREATH: a definitive classification of cell types requires more than extracellular recording can give Quotation withheld because this record is not cleared for redistribution. with the differences statistically highly significant but nevertheless not very large, and it is important to remember that Quotation withheld because this record is not cleared for redistribution. THE CONTRIBUTION IS MEASURING SOMETHING A PREDECESSOR ASSERTED: independence across overlapping assemblies was proposed but never demonstrated quantitatively Quotation withheld because this record is not cleared for redistribution. human hippocampal neurons look categorical and context-independent, which contrasts sharply with this result Quotation withheld because this record is not cleared for redistribution. AND THE DISAGREEMENT IS ATTRIBUTED TO A VARIABLE ONE LITERATURE NEVER VARIED: in the human studies the subjects were always tested in just a single location Quotation withheld because this record is not cleared for redistribution. odour studies had already reported location-dependent hippocampal responses, and this extends them to a neuron-by-neuron prediction failure across places Quotation withheld because this record is not cleared for redistribution. the same design had already been used with tactile stimuli by the same group, with the same independence result Quotation withheld because this record is not cleared for redistribution. auditory input reaches the hippocampus only very indirectly, and the structure is stated not to be a sensory one Quotation withheld because this record is not cleared for redistribution. the context dependence is said to fit an object-in-place account binding salient events to where they happened Quotation withheld because this record is not cleared for redistribution. artificial vowels were chosen as a more naturalistic stimulus class than pure tones Quotation withheld because this record is not cleared for redistribution. with formant spacing set well above the published threshold where rats reach plateau discrimination performance Quotation withheld because this record is not cleared for redistribution. the two platforms differed only in floor texture, position and orientation Quotation withheld because this record is not cleared for redistribution. and only well-isolated units with a clear refractory period were kept, with two quantitative separation measures on top of manual inspection Quotation withheld because this record is not cleared for redistribution. sound-sensitive neurons sound-sensitive neurons Quotation withheld because this record is not cleared for redistribution. response direction-sensitive neurons response direction-sensitive neurons Quotation withheld because this record is not cleared for redistribution. response direction response direction Quotation withheld because this record is not cleared for redistribution. information information Quotation withheld because this record is not cleared for redistribution. test test Quotation withheld because this record is not cleared for redistribution. independent independent Quotation withheld because this record is not cleared for redistribution. vowel vowel Quotation withheld because this record is not cleared for redistribution. putative pyramidal cells putative pyramidal cells Quotation withheld because this record is not cleared for redistribution. putative interneurons putative interneurons Quotation withheld because this record is not cleared for redistribution. sound identity sound identity Quotation withheld because this record is not cleared for redistribution. spatial context spatial context Quotation withheld because this record is not cleared for redistribution. sensitivity to sound identity sensitivity to sound identity Quotation withheld because this record is not cleared for redistribution. behavioral context behavioral context Quotation withheld because this record is not cleared for redistribution. putative cell type putative cell type Quotation withheld because this record is not cleared for redistribution. sound sound Quotation withheld because this record is not cleared for redistribution. direction direction Quotation withheld because this record is not cleared for redistribution. reaction time reaction time Quotation withheld because this record is not cleared for redistribution. latency latency Quotation withheld because this record is not cleared for redistribution. 55 of 261 (21%) — proportion of analysed CA1 neurons significantly sensitive to sound identity Quotation withheld because this record is not cleared for redistribution. 113 of 261 (43%) — proportion of analysed neurons significantly sensitive to response direction (left vs right turn) Quotation withheld because this record is not cleared for redistribution. 0.12 bits — median mutual information about sound identity carried by sound-sensitive neurons (ceiling for a two-way discrimination is 1 bit) Quotation withheld because this record is not cleared for redistribution. 310 ms — median latency after sound onset at which neurons began carrying significant sound-identity information Quotation withheld because this record is not cleared for redistribution. 80.2% / 70.6% — median behavioural accuracy on the first vs the second training platform, showing incomplete transfer of the task across locations Quotation withheld because this record is not cleared for redistribution. 179 / 82 — number of units classified as putative pyramidal cells versus putative interneurons Quotation withheld because this record is not cleared for redistribution. 33% vs 16% — share of putative interneurons versus putative pyramidal cells that were sound sensitive Quotation withheld because this record is not cleared for redistribution. 0.12 bits — median sound identity information in sensitive neurons, against an upper limit of 1.0 for a two-way discrimination Quotation withheld because this record is not cleared for redistribution. 261 of the total of 429 — neurons surviving the reaction-time exclusion - the cost of guaranteeing that the two sounds were treated identically Quotation withheld because this record is not cleared for redistribution. 6% — neurons classified sound sensitive during passive listening, against an expected false-alarm rate of 5 percent Quotation withheld because this record is not cleared for redistribution. 310 ms — median latency at which sound information first appears Quotation withheld because this record is not cleared for redistribution. 33% — putative interneurons carrying sound information, against 16 percent of putative pyramidal cells Quotation withheld because this record is not cleared for redistribution. 14% of cases — sessions discarded because the two sounds sharing a response produced different reaction times Quotation withheld because this record is not cleared for redistribution.

The full text of this article is not redistributable, so it is not included here. The evidence sentences are withheld with it; the tag layer and its grounding status remain. The article itself is at https://doi.org/10.1152/jn.00404.2011.