Executive Functions in Birds
Round 1
Reviewer 1 Report
I think this is a very nice and useful review. However, I noticed some references are missing and I think for a review completeness is important, so I have taken the liberty of suggesting them below:
p. 8 line 355 and elsewhere e.g. p. 9: On detour tasks the authors missed some relevant references for birds: Regolin et al. (1995). Detour behaviour in the domestic chick: Searching for a disappearing prey or a disappearing social partner. Animal Behaviour, 50: 203-211. Regolin et al. (1994). Perceptual and motivational aspects of detour behaviour in young chicks. Animal Behaviour, 47: 123-131; Vallortigara, G., Regolin, L. (2002). Facing an obstacle: Lateralization of object and spatial cognition. In: Comparative Vertebrate Lateralization (R.J. Andrew and L.J. Rogers, eds.), pp. 383-444, Cambridge: Cambridge University Press; Vallortigara, G. (2006). The Cognitive Chicken: Visual and Spatial Cognition in a Non-Mammalian Brain. In: Comparative Cognition: Experimental Explorations of Animal Intelligence (E.A. Wasserman & T.R. Zentall, eds.), pp. 41-58, Oxford University Press, Oxford, U.K.
AS to working memory classical work on delayed responses should be alsdo considered: Vallortigara et al. (1998). Delayed search for a concealed imprinted object in the domestic chick. Animal Cognition, 1: 17-24. Regolin et al. (2005). Delayed search for a social and a non-social goal object by the young domestic chick (Gallus gallus). Animal Behaviour, 70: 855-864.
Author Response
I think this is a very nice and useful review. However, I noticed some references are missing and I think for a review completeness is important, so I have taken the liberty of suggesting them below:
- 8 line 355 and elsewhere e.g. p. 9: On detour tasks the authors missed some relevant references for birds:
Regolin et al. (1995). Detour behaviour in the domestic chick: Searching for a disappearing prey or a disappearing social partner. Animal Behaviour, 50: 203-211.
Regolin et al. (1994). Perceptual and motivational aspects of detour behaviour in young chicks. Animal Behaviour, 47: 123-131;
Vallortigara, G., Regolin, L. (2002). Facing an obstacle: Lateralization of object and spatial cognition. In: Comparative Vertebrate Lateralization (R.J. Andrew and L.J. Rogers, eds.), pp. 383-444, Cambridge: Cambridge University Press;
Vallortigara, G. (2006). The Cognitive Chicken: Visual and Spatial Cognition in a Non-Mammalian Brain. In: Comparative Cognition: Experimental Explorations of Animal Intelligence (E.A. Wasserman & T.R. Zentall, eds.), pp. 41-58, Oxford University Press, Oxford, U.K.
AS to working memory classical work on delayed responses should be alsdo considered:
Vallortigara et al. (1998). Delayed search for a concealed imprinted object in the domestic chick. Animal Cognition, 1: 17-24.
Regolin et al. (2005). Delayed search for a social and a non-social goal object by the young domestic chick (Gallus gallus). Animal Behaviour, 70: 855-864.
This has now been amended and we have included the relevant references into the revised version of our article. We thank the Reviewer for directing us towards these references.
Reviewer 2 Report
Please add a new subchapter containing all the ,,Future directions in......''.
A chapter containing a comparison between birds and mammals could be valuable for this work.
Author Response
Please add a new subchapter containing all the ,,Future directions in......''.
We have now added such a subchapter (p.22, starting at line 1977). Now sections on inhibition, working memory and cognitive flexibility are concluded with brief summaries that no longer comprise general future directions. Instead, the brief summaries contain a short recapitulation of hitherto presented research and a link to the next section.
A chapter containing a comparison between birds and mammals could be valuable for this work.
We included a chapter containing a comparison between birds and humans in order to clarify terms and tasks used in these two groups (pp. 6-8, lines 256-437).
Reviewer 3 Report
The goal of this review is to provide an organized overview of how specific executive functions, inhibition, updating, and shifting have thus far been studied in birds. They structure the review by providing a brief overview of comparative research on executive functions throughout the years, how they conducted a literature search, the brain regions that support this behavior, and then they summarize relevant research in birds under the categories mentioned previously.
The overview of tasks used thus far in birds (sections 3-5) are quite good and clear. Each task is clearly laid out and described. For the most part, I agree with how tasks are categorized and there is only one section where I find research is missing (shifting).
I also admire the ambition of writing such a review, this is a huge body of literature that spans many different fields of research. Unfortunately, this review does suffer from clarity issues. The second section in particular, I had trouble determining what exactly the authors were referring to and the overall goal. The header of section 2 is ‘Neural correlates of executive functions in the avian brain’, which accords with the first five paragraphs in this section. The goal of the remaining paragraphs in this section is not clear to me, which I explain in detail below. It may help, in general, to have a separate section that briefly compares and contrasts how these executive functions are conceptualized in humans versus animals, or birds specifically,
This paper also ends a bit abruptly. The authors stress how important it is to control or track almost all other variables to account for differences between species. They also stress contextual factors of the procedures themselves. What they actually hope readers get from this paper is not clearly stated. They also do not have any specific suggestions for what they hope to see in the field. A review paper by Shaw and Schmelz (2017) lays out very clear suggestions and could be helpful.
Finally, I think this paper would be strengthened by an additional paragraph that more directly compares how these processes are assessed in humans compared to birds. I’m fully aware this review is aimed towards avian researchers, but since the concept of these executive functions originated in human cognitive research, I think it should be addressed. As stated in this review, some of the delay tasks used to assess working memory in birds (pigeons in particular) are assessing short term memory, not updating, if we use human cognitive research as a guide. I elaborate on this in more detail below, but in general that will make comparisons difficult if tasks using the same name (working memory) are assessing different processes (updating versus storage).
Page 6, second paragraph, lines 231-243: I don’t fully understand the difference in how neurocognitive and behavioral studies are conceptualizing executive functions. What is the difference between taking ‘different forms’ in neurocognitive studies and ‘core cognitive processes’ in behavioral studies? I also find the introduction of Miyake and Diamond’s work slightly awkward and confusing. It’s not clear if you, the authors, are placing the previous work conducted in birds into the EF framework by Miyake and Diamond or if this connection was already made by the avian researchers.
Page 6, Second and third paragraph, lines 243-256: I don’t fully understand why you discuss the difference in how inhibition is defined by Miyake and Diamond in the second paragraph. It seems to signal a shift in how EF are described by these two researchers, and if so, it would be better to start a new paragraph. Part of my confusion comes from line 254, ‘...the definitions are similar in both accounts...’. When you say both, are you referring to Miyake and Diamond or are you referring to the neurocognitive and behavioral lines of research? I think it would also be helpful to clarify ‘updating’ here in the sentence about working memory. While updating is listed as one of the processes supporting working memory, it’s not clear that updating is the main process referred to in the human EF literature.
Pages 6-7, third paragraph, lines 256-272: From the definition of shifting, it sounds like the goal of the second and third paragraphs are to contrast the human literature with the animal or comparative literature. However, this is quite confusing since two different definitions of switching are presented here and are seemingly presented as contradicting or contrasting theoretical views. Then the next sentence seems to ignore that difference to present the underlying processes and provide an example that seems to accord to the first definition only. It’s not clear if this example is from the human or animal literature. My impression is that this is an example from the animal literature since the serial reversal learning task described in the next sentence matches the example given. Overall, I think the shifting section in particular needs to be better organized to clarify when the authors are referring to human research, which human research, and animal research.
I have an additional comment about the animal research presented in this paragraph. I personally have not seen this particular task (in context A, perform action A; in context B, perform action B), ever presented as a reversal learning task. When I have looked up a serial reversal learning task, the stimuli and context remain the same, but the contingencies reverse without any additional signal to the animal. From my reading of the literature, the most crucial aspect of a reversal learning task is that something that has been learned previously is now reversed, not switching between two learned behaviors. This concern extends to the first paragraph in page 7.
Page 8, lines 351-353: I think it is important to include the sentence about how motor self-regulation and self-control are dissociable in humans after describing these two concepts. This implies that inhibition is not unitary, particularly when using these two types of tasks.
Page 9, line 362; Page 12, line 404: On page 9, the subheading is 3.1.1. Detour tasks. On page 12, line 404, the subheading is 3.1.2. Detour tasks.
Page 10, table; Page 13, lines 426-454: Including reversal learning under the ‘inhibition’ category further confuses the point as to the reversal learning task you described as shifting and the reversal learning tasks commonly used in the literature. This section (3.1.3.1.) indicates that you do know this literature well, but I’m even more confused as to the objective of page 6.
Page 8, lines 317-327, Page 15, lines 528-569: Overall, I like this section on inhibition, but I think the paragraph about individual differences impacting cross species comparisons would be better in the ‘future directions’ section. I think this ‘future directions’ section could be even stronger with more specific recommendations. It’s a nice summary and brings up interesting comparisons across studies, but it’s not clear where you think the field should go or where you think it is going.
Page 16, lines 590-595: ‘Although in avian research, working memory is conceptualized as a cognitive module that is separate from inhibitory control...’, I think this sentence is an oversimplification. Reading the cited paper (81), they describe the results in the context of being able to maintain a representation during its physical absence. So, they are discussing the various neural evidence for delay-type tasks specifically and even state that it is more similar to initial definitions of short-term memory.
Further, even though they describe working memory as a cognitive module, they acknowledge it has subcomponents. The multi-faceted nature of working memory and working memory tasks are also acknowledged in other avian research papers.
The first conceptualization, with inhibition, WM, and shifting as separable constructs, is also consistent with Miyake’s research of separable, but overlapping constructs. Therefore, I’m not sure what is being contrasted.
Page 21, line 853: Similar to earlier comment, I’m not sure the term ‘reversal learning’ is the most appropriate to describe the previous tasks, where subjects had to switch between two different behaviors.
Page 21, lines 853-861: The section titled ‘Ranking tasks’ describes a ‘hierarchy’ task that strongly reminds me of transitivity research conducted with pigeons. This may be an example of switching, but there are other theoretical motivations for this task.
Pages 21-22, lines 868-883: This phrasing is used throughout the manuscript, but the way shifting is described makes it sound like it is just a combination of inhibition and working memory. I don’t think this is intentional, but it doesn’t fully acknowledge how shifting is also unique from these two processes, at least in humans. Additionally, while you state that these tasks may be better at identifying cognitive differences between species, I’m not sure that’s true. I don’t know how shifting tasks would be immune from the same contextual variables that haunt all cognitive tasks and cross species comparisons. To elaborate on this point, even if consistent cross species differences were found in shifting tasks, they would need to investigate why at the cognitive level. This would bring comparisons back ‘down’ to working memory and inhibition.
You also state that the avian field should develop more unique shifting tasks. I agree in principle, but the concept of shifting is conceptually narrow and I’m not convinced that the hierarchy tasks are assessing shifting.
Page 22, lines 900-908: This critique of inhibitory control tasks in particular is not unique to inhibitory control tasks or to avian research. The weak correlations between tasks could be due to the fact that they assess different underlying processes or assess similar processes to different degrees. The different tasks used to assess working memory in humans is a nice example of this debate in another field.
Pages 22-24: This table is a bit tricky to read. Would it be possible to insert a landscape page or flip the orientation of the table?
Pages 24-25, lines 923-935: I’m surprised the research conducted by Ashton et al., 2018 isn’t referenced here, considering it is included in the references list. That showed robust correlations across different cognitive tasks and extracted a strong ‘g’ like factor. There is other research conducted by Boogert and Anderson with song sparrow that did not show similar results. A follow up study by Soha et al. (2019) demonstrated performance in song sparrows was not reliable across years in the same subject for the same task. These references provide additional nuance to potential differences across species. I’m not sure it is worth bringing up ‘g’ in this paper due to the number of statistical and methodological issues with it (as outlined in reference 38), but addressing how reliability may differs across species is interesting. This may not be an issue with the task, but a genuine difference across species.
Author Response
The goal of this review is to provide an organized overview of how specific executive functions, inhibition, updating, and shifting have thus far been studied in birds. They structure the review by providing a brief overview of comparative research on executive functions throughout the years, how they conducted a literature search, the brain regions that support this behavior, and then they summarize relevant research in birds under the categories mentioned previously.
The overview of tasks used thus far in birds (sections 3-5) are quite good and clear. Each task is clearly laid out and described. For the most part, I agree with how tasks are categorized and there is only one section where I find research is missing (shifting).
We thank the Reviewer for these remarks and reviewing our manuscript. We truly appreciate the Reviewer’s generally positive feedback.
I also admire the ambition of writing such a review, this is a huge body of literature that spans many different fields of research. Unfortunately, this review does suffer from clarity issues. The second section in particular, I had trouble determining what exactly the authors were referring to and the overall goal. The header of section 2 is ‘Neural correlates of executive functions in the avian brain’, which accords with the first five paragraphs in this section. The goal of the remaining paragraphs in this section is not clear to me, which I explain in detail below. It may help, in general, to have a separate section that briefly compares and contrasts how these executive functions are conceptualized in humans versus animals, or birds specifically,
We found this comment very helpful, as it prompted us to clarify the relevant paragraphs. In general, we do not want to suggest that EFs are conceptualized differently in human vs. avian research, quite the contrary. In humans, two broad conceptualizations are prevalent, one focused on “executive control” and another focused on “executive functions”. These two conceptualizations are represented in avian research, as the neurocognitive studies typically refer to executive control, and the behavioural studies typically refer to executive functions. We hope that this has now become clearer in the revised section 2.2., entitled “Conceptualizations of EFs in humans and birds” (p. 6-7; lines 256-337). In general, we have reorganized entire section 2 to accommodate the discussion of the relevant frameworks and EF tasks in human research.
This paper also ends a bit abruptly. The authors stress how important it is to control or track almost all other variables to account for differences between species. They also stress contextual factors of the procedures themselves. What they actually hope readers get from this paper is not clearly stated. They also do not have any specific suggestions for what they hope to see in the field. A review paper by Shaw and Schmelz (2017) lays out very clear suggestions and could be helpful.
We thank the Reviewer for directing us toward the paper by Shaw and Schmelz. Guided by that paper, we have now rewritten the entire section 6.2. (now: Future directions and conclusions, pp. 22-28; lines 1997-2116)).
Finally, I think this paper would be strengthened by an additional paragraph that more directly compares how these processes are assessed in humans compared to birds. I’m fully aware this review is aimed towards avian researchers, but since the concept of these executive functions originated in human cognitive research, I think it should be addressed. As stated in this review, some of the delay tasks used to assess working memory in birds (pigeons in particular) are assessing short term memory, not updating, if we use human cognitive research as a guide. I elaborate on this in more detail below, but in general that will make comparisons difficult if tasks using the same name (working memory) are assessing different processes (updating versus storage).
We agree with this comment, and we thank the Reviewer for pointing this out. In section 2.3. EF tasks in humans (pp. 7-8; lines. 338-437), we are now discussing different task categories. Following research on humans, we discussed simple and complex working memory tasks, i.e., short-term memory tasks and “true” working memory tasks, respectively, in this section.
Page 6, second paragraph, lines 231-243: I don’t fully understand the difference in how neurocognitive and behavioral studies are conceptualizing executive functions. What is the difference between taking ‘different forms’ in neurocognitive studies and ‘core cognitive processes’ in behavioral studies? I also find the introduction of Miyake and Diamond’s work slightly awkward and confusing. It’s not clear if you, the authors, are placing the previous work conducted in birds into the EF framework by Miyake and Diamond or if this connection was already made by the avian researchers.
We have now amended this section, highlighting differences in terminologies and frameworks between neurocognitive and behavioural studies. We have also clarified that “Diamond’s definition of inhibition seems to be more prevalent in avian research, and, therefore, will be used to organize relevant findings in this review paper” (lines 327-329) to address the second part of the Reviewer’s comment.
Page 6, Second and third paragraph, lines 243-256: I don’t fully understand why you discuss the difference in how inhibition is defined by Miyake and Diamond in the second paragraph. It seems to signal a shift in how EF are described by these two researchers, and if so, it would be better to start a new paragraph. Part of my confusion comes from line 254, ‘...the definitions are similar in both accounts...’. When you say both, are you referring to Miyake and Diamond or are you referring to the neurocognitive and behavioral lines of research? I think it would also be helpful to clarify ‘updating’ here in the sentence about working memory. While updating is listed as one of the processes supporting working memory, it’s not clear that updating is the main process referred to in the human EF literature.
We have now reworked this part of the manuscript in order to clarify the differences between Diamond’s and Miyake and colleagues’ definitions (section 2.2, pp. 6-7). We have also introduced another section (2.3, pp. 7-8), in which working memory tasks for humans are discussed. It is now clearly stated that “updating” is measured only in complex, but not simple, working memory tasks for humans.
Pages 6-7, third paragraph, lines 256-272: From the definition of shifting, it sounds like the goal of the second and third paragraphs are to contrast the human literature with the animal or comparative literature. However, this is quite confusing since two different definitions of switching are presented here and are seemingly presented as contradicting or contrasting theoretical views. Then the next sentence seems to ignore that difference to present the underlying processes and provide an example that seems to accord to the first definition only. It’s not clear if this example is from the human or animal literature. My impression is that this is an example from the animal literature since the serial reversal learning task described in the next sentence matches the example given. Overall, I think the shifting section in particular needs to be better organized to clarify when the authors are referring to human research, which human research, and animal research.
This part of the manuscript has been reworked and is available in section 2.3 (p. 7). Based on human literature, we explicitly discern between response-shifting (reversal) tasks and attention-shifting (dimensional change) tasks (lines 336-337; 428-437).
I have an additional comment about the animal research presented in this paragraph. I personally have not seen this particular task (in context A, perform action A; in context B, perform action B), ever presented as a reversal learning task. When I have looked up a serial reversal learning task, the stimuli and context remain the same, but the contingencies reverse without any additional signal to the animal. From my reading of the literature, the most crucial aspect of a reversal learning task is that something that has been learned previously is now reversed, not switching between two learned behaviors. This concern extends to the first paragraph in page 7.
We acknowledge that these statements were confusing, and we have now removed them. We no longer use the term “reversal learning”; instead, we switched to “response shifting/response reversal”, commonly used in human literature. This is presented as follows: “Response shifting (reversal) tasks typically require the individual to switch between two arbitrary stimulus-response contingencies. For instance, the individual is repeatedly trained to retrieve a reward from one location, and thereafter needs to inhibit this response in favour of retrieval from another location (spatial reversal task; A-not-B task; [106]).” (p. 8, lines 429-433).
Serial reversal tasks are defined as follows: “In contrast to serial reversal tasks, for example, where the animal needs to shift between two context-response contingencies, in the repeated acquisition procedure, the animal needs to learn a new response sequence to the same context each time they master the previously correct response sequence [115; 118].” (p. 8, lines 447-450).
Page 8, lines 351-353: I think it is important to include the sentence about how motor self-regulation and self-control are dissociable in humans after describing these two concepts. This implies that inhibition is not unitary, particularly when using these two types of tasks.
Such sentence is now available in section 2.3 (EF tasks in humans, pp. 7-8): “Simple response inhibition tasks involve inhibiting a prepotent motor response, for instance, reaching toward a transparent surface in favour of reaching to, e.g., a side opening (motor self-regulation), or reaching for an immediate attractive reward in favour of waiting for a delayed but more attractive reward (delayed self-gratification). Both these tasks were adopted by avian EF research. Motor inhibition tasks were termed motor self-regulation (detour) tasks, and delayed self-gratification tasks were termed self-control tasks.”
Page 9, line 362; Page 12, line 404: On page 9, the subheading is 3.1.1. Detour tasks. On page 12, line 404, the subheading is 3.1.2. Detour tasks.
This has now been amended.
Page 10, table; Page 13, lines 426-454: Including reversal learning under the ‘inhibition’ category further confuses the point as to the reversal learning task you described as shifting and the reversal learning tasks commonly used in the literature. This section (3.1.3.1.) indicates that you do know this literature well, but I’m even more confused as to the objective of page 6.
We have now moved these tasks to the subsections on Cognitive flexibility (section 5, pp. 20-21; lines 1822-1888).
Page 8, lines 317-327, Page 15, lines 528-569: Overall, I like this section on inhibition, but I think the paragraph about individual differences impacting cross species comparisons would be better in the ‘future directions’ section. I think this ‘future directions’ section could be even stronger with more specific recommendations. It’s a nice summary and brings up interesting comparisons across studies, but it’s not clear where you think the field should go or where you think it is going.
We have now developed the section on future directions, including the reference to the paper suggested by the Reviewer (Shaw & Schmelz, 2017) (pp. 22-28, lines 1984-2123).
Page 16, lines 590-595: ‘Although in avian research, working memory is conceptualized as a cognitive module that is separate from inhibitory control...’, I think this sentence is an oversimplification. Reading the cited paper (81), they describe the results in the context of being able to maintain a representation during its physical absence. So, they are discussing the various neural evidence for delay-type tasks specifically and even state that it is more similar to initial definitions of short-term memory.
Further, even though they describe working memory as a cognitive module, they acknowledge it has subcomponents. The multi-faceted nature of working memory and working memory tasks are also acknowledged in other avian research papers.
The first conceptualization, with inhibition, WM, and shifting as separable constructs, is also consistent with Miyake’s research of separable, but overlapping constructs. Therefore, I’m not sure what is being contrasted.
We thank the Reviewer for drawing our attention to this issue. We agree that this part of the manuscript was oversimplified, and we have now removed it from this section. We have, instead, incorporated a discussion of various EF (and WM) conceptualizations in sections 2.2 (lines 265-319) and 2.3 (lines 355-427).
Page 21, line 853: Similar to earlier comment, I’m not sure the term ‘reversal learning’ is the most appropriate to describe the previous tasks, where subjects had to switch between two different behaviors.
We followed the nomenclature used in the referred studies, but we have now changed “reversal learning” to “response reversal”.
Page 21, lines 853-861: The section titled ‘Ranking tasks’ describes a ‘hierarchy’ task that strongly reminds me of transitivity research conducted with pigeons. This may be an example of switching, but there are other theoretical motivations for this task.
We have now removed these tasks altogether, given Reviewer’s suggestion below, regarding doubts whether hierarchy tasks measure cognitive flexibility.
Pages 21-22, lines 868-883: This phrasing is used throughout the manuscript, but the way shifting is described makes it sound like it is just a combination of inhibition and working memory. I don’t think this is intentional, but it doesn’t fully acknowledge how shifting is also unique from these two processes, at least in humans. Additionally, while you state that these tasks may be better at identifying cognitive differences between species, I’m not sure that’s true. I don’t know how shifting tasks would be immune from the same contextual variables that haunt all cognitive tasks and cross species comparisons. To elaborate on this point, even if consistent cross species differences were found in shifting tasks, they would need to investigate why at the cognitive level. This would bring comparisons back ‘down’ to working memory and inhibition.
We have now removed these statements.
You also state that the avian field should develop more unique shifting tasks. I agree in principle, but the concept of shifting is conceptually narrow and I’m not convinced that the hierarchy tasks are assessing shifting.
We have now removed this task altogether, as we agree that it is often used as a transitive inference task.
Page 22, lines 900-908: This critique of inhibitory control tasks in particular is not unique to inhibitory control tasks or to avian research. The weak correlations between tasks could be due to the fact that they assess different underlying processes or assess similar processes to different degrees. The different tasks used to assess working memory in humans is a nice example of this debate in another field.
We agree with this statement and we have now inserted this in the relevant paragraph.
Pages 22-24: This table is a bit tricky to read. Would it be possible to insert a landscape page or flip the orientation of the table?
We have now changed the layout of the table to a horizontal one.
Pages 24-25, lines 923-935: I’m surprised the research conducted by Ashton et al., 2018 isn’t referenced here, considering it is included in the references list. That showed robust correlations across different cognitive tasks and extracted a strong ‘g’ like factor. There is other research conducted by Boogert and Anderson with song sparrow that did not show similar results. A follow up study by Soha et al. (2019) demonstrated performance in song sparrows was not reliable across years in the same subject for the same task. These references provide additional nuance to potential differences across species. I’m not sure it is worth bringing up ‘g’ in this paper due to the number of statistical and methodological issues with it (as outlined in reference 38), but addressing how reliability may differs across species is interesting. This may not be an issue with the task, but a genuine difference across species.
We have missed these references here, but we have now inserted them, as all were present in the reference list (Boogert et al., 2011; Soha et al., 2019, too). We have also decided to retain the notion of “g” because it does come up in the referred literature, and we would like the reader to be ready for this notion when consulting specific papers.
Round 2
Reviewer 3 Report
Minor revisions
Overall I really appreciate the changes made and I am glad the authors found my feedback helpful. There is still one section that I think could be clarified, which is detailed below. Overall, I think the review is quite comprehensive, especially given the body of research, and will be helpful for future researchers.
Pages 8-9, lines 361-365 (very minor): You state that the context for the card sorting task changes after 10 responses, is this after 10 consecutive correct responses?
Page 9, lines 369-372: When discussing damage to the hippocampus, you state that they needed an increased number of trial before finding the correct response. I'm not sure how this is different from the effects seen when damaging the Wulst and LPO, since that also seemed to impair finding the correct response. How does the hipppocampal damage suggest difficulty in consolidation specifically?
Page 9, lines 373-374: In regards to the avian or pigeon hippocampus being involved with spatial information specifically, I don't disagree with this take - there is a lot of evidence to support it! However, since refs 124 and 126 mention that hippocampus damage also impairs autoshaping, it might be good to add a little more nuance. Further, Colombo has also shown that hippocampus damage can impair other forms of inhibition, like extinction learning. There is also an extremely recent paper from Damphousse, Miller, & Marrone (2022) with Japanese quail, showing an object memory impairment after hippocampus lesions.
Page 22, section 5.4, line 895 very minor typo 'pecies-specific' instead of species-specific
Author Response
Overall I really appreciate the changes made and I am glad the authors found my feedback helpful. There is still one section that I think could be clarified, which is detailed below. Overall, I think the review is quite comprehensive, especially given the body of research, and will be helpful for future researchers.
We thank Reviewer 3 for all comments shared with us in both this and the previous revision round.
Pages 8-9, lines 361-365 (very minor): You state that the context for the card sorting task changes after 10 responses, is this after 10 consecutive correct responses?
This is correct, we have now inserted the missing word at line 366.
Page 9, lines 369-372: When discussing damage to the hippocampus, you state that they needed an increased number of trial before finding the correct response. I'm not sure how this is different from the effects seen when damaging the Wulst and LPO, since that also seemed to impair finding the correct response. How does the hipppocampal damage suggest difficulty in consolidation specifically?
We have now reworked this section. The bottom line should be as follows: the LPO and the Wulst are crucial when acquiring the correct response, likely due to their involvement in inhibition of incorrect responses, and the hippocampal formation is crucial when retaining and retrieving the correct response (lines 369-379). We have also directed readers toward a more detailed discussion of this matter in reference no. 115.
Page 9, lines 373-374: In regards to the avian or pigeon hippocampus being involved with spatial information specifically, I don't disagree with this take - there is a lot of evidence to support it! However, since refs 124 and 126 mention that hippocampus damage also impairs autoshaping, it might be good to add a little more nuance. Further, Colombo has also shown that hippocampus damage can impair other forms of inhibition, like extinction learning. There is also an extremely recent paper from Damphousse, Miller, & Marrone (2022) with Japanese quail, showing an object memory impairment after hippocampus lesions.
We thank the Reviewer for these remarks, and we certainly agree that the take on the hippocampal formation was not sufficiently nuanced. Given that the findings of Damphousse and colleagues resulted from damage to both the hippocampal formation and the area parahippocampalis, this is how we framed these findings in the text: “Damage to the hippocampal formation may result rather in spatial working memory than non-spatial working memory impairments [124-128] but note that damage to the hippocampal formation (and the adjacent area parahippocampalis) was also shown to impair acquisition of an autoshaped response (Domestic Pigeon, Columba livia domestica, [124; 126; 129] and object recognition (Japanese Quail, Coturnix japonica [130])” at lines 369-384. To our knowledge, APH is typically not considered a part of the hippocampal formation (e.g., Atoji & Wild, 2006; Székely, 1999).
Page 22, section 5.4, line 895 very minor typo 'pecies-specific' instead of species-specific
We have now amended this; we thank the Reviewer for their attentiveness.
